{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,13]],"date-time":"2026-07-13T15:17:28Z","timestamp":1783955848619,"version":"3.55.0"},"reference-count":46,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T00:00:00Z","timestamp":1669852800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Muscle strain injuries (MSIs) in the hamstrings are among the most prevalent injuries in elite soccer. We aimed to examine the relation between biomechanical maladaptation in eccentric strength and neuromuscular factors separated by their time and frequency domains.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>20 elite soccer players with a previous history of unilateral MSI in the M. biceps femoris (BF) long head and 20 without MSI participated. Knee flexion torques, rate of torque development (RTD) and electromyographic signals (EMG) of the BF, the M. semitendinosus (SMT) and knee extensors were obtained during unilateral maximal eccentric knee flexions performed at slow (30\u00b0\/s) and fast (120\u00b0\/s) angular speeds. Root mean squares and mean power frequency (MF) was calculated.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>In the group with a history of MSI, reduced maximal eccentric flexion torque (slow eccentrics -8\u00b111, p&lt;0.05; fast eccentrics -18\u00b113 N*m, p&lt;0.05) and RTD (-33\u00b128 N*m\/s, p&lt;0.05; -95\u00b147 N*m\/s, p&lt;0.05) concomitantly occurred with diminished agonistic myoelectrical activities (-4\u00b15% of MVC, p&lt;0.05; -10\u00b17% of MVC, p&lt;0.05) and MFs (-24\u00b113 Hz, p&lt;0.05; -24\u00b118 Hz, p&lt;0.05) in the BF. Simultaneously, antagonistic myoelectric activity was elevated (+4\u00b13% of MVC, p&lt;0.05; +3\u00b13% of MVC, p&lt;0.05) in MSI affected legs as compared to unaffected legs for both eccentric contractions. Deficits in myoelectrical activity (r<jats:sup>2<\/jats:sup> = 0.715, p&lt;0.05; r<jats:sup>2<\/jats:sup> = 0.601, p&lt;0.05) and MF (r<jats:sup>2<\/jats:sup> = 0.484, p&lt;0.05; r<jats:sup>2<\/jats:sup> = 0.622, p&lt;0.05) correlated with deficits in maximal torque in the affected leg in the MSI group. Analysis of SMT demonstrated no significant differences.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusion<\/jats:title>\n<jats:p>Positive relationships between neuromuscular deficits and the reduced eccentric strength profile underpin neuronal inhibition after MSI. This persistent involvement of dysfunctional synergist and antagonist neural hamstring function in strength weakness is of clinical relevance in sports medicine for prevention and rehabilitation.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0277949","type":"journal-article","created":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T20:11:13Z","timestamp":1669925473000},"page":"e0277949","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Neuromuscular characteristics of agonists and antagonists during maximal eccentric knee flexion in soccer players with a history of hamstring muscle injuries"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5325-0711","authenticated-orcid":true,"given":"Ramona","family":"Ritzmann","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Str\u00fctt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ignacio","family":"Torreno","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janine","family":"Riesterer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Centner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5432-4786","authenticated-orcid":true,"given":"Luis","family":"Suarez-Arrones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,12,1]]},"reference":[{"issue":"3","key":"pone.0277949.ref001","doi-asserted-by":"crossref","first-page":"209","DOI":"10.2165\/11594800-000000000-00000","article-title":"Hamstring strain injuries: factors that lead to injury and re-injury","volume":"42","author":"DA Opar","year":"2012","journal-title":"Sports Med"},{"issue":"6","key":"pone.0277949.ref002","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1177\/03635465030310063701","article-title":"Diagnostic and prognostic value of clinical findings in 83 athletes with posterior thigh injury: comparison of clinical findings with magnetic resonance imaging documentation of hamstring muscle strain","volume":"31","author":"GM Verrall","year":"2003","journal-title":"Am J Sports Med"},{"issue":"1","key":"pone.0277949.ref003","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1136\/bjsm.2002.002352","article-title":"The Football Association Medical Research Programme: an audit of injuries in professional football\u2014analysis of hamstring injuries","volume":"38","author":"C Woods","year":"2004","journal-title":"Br J Sports Med"},{"issue":"1\u20132","key":"pone.0277949.ref004","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.jsams.2006.03.007","article-title":"Assessment of player performance following return to sport after hamstring muscle strain injury","volume":"9","author":"GM Verrall","year":"2006","journal-title":"J Sci Med Sport"},{"issue":"6","key":"pone.0277949.ref005","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1136\/bjsm.36.6.436","article-title":"The Football Association Medical Research Programme: an audit of injuries in professional football-analysis of preseason injuries","volume":"36","author":"C Woods","year":"2002","journal-title":"Br J Sports Med"},{"issue":"12","key":"pone.0277949.ref006","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1136\/bjsports-2015-095359","article-title":"Hamstring injuries have increased by 4% annually in men\u2019s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study","volume":"50","author":"J Ekstrand","year":"2016","journal-title":"Br J Sports Med"},{"issue":"24","key":"pone.0277949.ref007","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.1136\/bjsports-2015-095362","article-title":"Short biceps femoris fascicles and eccentric knee flexor weakness increase the risk of hamstring injury in elite football (soccer): a prospective cohort study","volume":"50","author":"RG Timmins","year":"2016","journal-title":"Br J Sports Med"},{"issue":"3","key":"pone.0277949.ref008","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/j.jshs.2017.04.001","article-title":"Rehabilitation and return to sport after hamstring strain injury","volume":"6","author":"LN Erickson","year":"2017","journal-title":"J Sport Health Sci"},{"issue":"14","key":"pone.0277949.ref009","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1055\/s-0034-1375696","article-title":"The rate of torque development: a unique, non-invasive indicator of eccentric-induced muscle damage?","volume":"35","author":"ND Jenkins","year":"2014","journal-title":"Int J Sports Med."},{"issue":"8","key":"pone.0277949.ref010","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1016\/S0268-0033(02)00070-0","article-title":"Relationship between wire EMG activity, muscle length, and torque of the hamstrings","volume":"17","author":"O Mohamed","year":"2002","journal-title":"Clin Biomech (Bristol, Avon)."},{"issue":"12","key":"pone.0277949.ref011","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1080\/02640414.2017.1375548","article-title":"Differences in hamstring activation characteristics between the acceleration and maximum-speed phases of sprinting","volume":"36","author":"A Higashihara","year":"2018","journal-title":"J Sports Sci"},{"key":"pone.0277949.ref012","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1113\/jphysiol.1978.sp012265","article-title":"Muscle spindle activity in man during shortening and lengthening contractions","volume":"277","author":"D Burke","year":"1978","journal-title":"The Journal of physiology"},{"key":"pone.0277949.ref013","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.clinbiomech.2018.07.009","article-title":"Is neuromuscular inhibition detectable in elite footballers during the Nordic hamstring exercise?","volume":"58","author":"L Blandford","year":"2018","journal-title":"Clin Biomech (Bristol, Avon)"},{"issue":"6","key":"pone.0277949.ref014","first-page":"666","article-title":"Muscle activation patterns in the Nordic hamstring exercise: Impact of prior strain injury. Scandinavian Journal of Medicine &","volume":"26","author":"MN Bourne","year":"2016","journal-title":"Science in Sports"},{"issue":"3","key":"pone.0277949.ref015","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1016\/j.jelekin.2012.11.004","article-title":"Knee flexor strength and bicep femoris electromyographical activity is lower in previously strained hamstrings","volume":"23","author":"DA Opar","year":"2013","journal-title":"J Electromyogr Kinesiol"},{"issue":"2","key":"pone.0277949.ref016","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1136\/bjsm.30.2.156","article-title":"Eccentric and concentric isokinetic knee flexion and extension: a reliability study using the Cybex 6000 dynamometer","volume":"30","author":"RC Li","year":"1996","journal-title":"Br J Sports Med"},{"issue":"20","key":"pone.0277949.ref017","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1136\/bjsports-2014-094569","article-title":"Strategic Assessment of Risk and Risk Tolerance (StARRT) framework for return-to-play decision-making","volume":"49","author":"I. Shrier","year":"2015","journal-title":"Br J Sports Med"},{"issue":"3","key":"pone.0277949.ref018","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/j.jelekin.2012.12.006","article-title":"The role of neuromuscular inhibition in hamstring strain injury recurrence","volume":"23","author":"JJ Fyfe","year":"2013","journal-title":"J Electromyogr Kinesiol"},{"issue":"6","key":"pone.0277949.ref019","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1136\/bjsm.35.6.435","article-title":"Clinical risk factors for hamstring muscle strain injury: a prospective study with correlation of injury by magnetic resonance imaging","volume":"35","author":"GM Verrall","year":"2001","journal-title":"Br J Sports Med"},{"issue":"17","key":"pone.0277949.ref020","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1136\/bjsports-2016-096849","article-title":"Epidemiology of injuries in judo: a cross-sectional survey of severe injuries based on time loss and reduction in sporting level","volume":"52","author":"R Akoto","year":"2018","journal-title":"Br J Sports Med"},{"issue":"5","key":"pone.0277949.ref021","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1111\/cpf.12495","article-title":"Physiological and methodological aspects of rate of force development assessment in human skeletal muscle","volume":"38","author":"D Rodr\u00edguez-Rosell","year":"2018","journal-title":"Clin Physiol Funct Imaging"},{"issue":"4","key":"pone.0277949.ref022","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1152\/japplphysiol.00283.2002","article-title":"Increased rate of force development and neural drive of human skeletal muscle following resistance training","volume":"93","author":"P Aagaard","year":"2002","journal-title":"Journal of applied physiology (Bethesda, Md: 1985)."},{"issue":"1","key":"pone.0277949.ref023","article-title":"Muscle Length of the Hamstrings Using Ultrasonography Versus Musculoskeletal Modelling.","volume":"6","author":"E Kellis","year":"2021","journal-title":"J Funct Morphol Kinesiol"},{"issue":"3","key":"pone.0277949.ref024","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1249\/01.MSS.0000117165.75832.05","article-title":"Predicting hamstring strain injury in elite athletes","volume":"36","author":"CL Brockett","year":"2004","journal-title":"Med Sci Sports Exerc"},{"issue":"4","key":"pone.0277949.ref025","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1111\/j.1748-1716.1995.tb09927.x","article-title":"Isokinetic hamstring\/quadriceps strength ratio: influence from joint angular velocity, gravity correction and contraction mode","volume":"154","author":"P Aagaard","year":"1995","journal-title":"Acta Physiol Scand"},{"issue":"4","key":"pone.0277949.ref026","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1159\/000047908","article-title":"In vivo measurement of fascicle length and pennation angle of the human biceps femoris muscle","volume":"169","author":"GS Chleboun","year":"2001","journal-title":"Cells Tissues Organs"},{"issue":"1","key":"pone.0277949.ref027","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1007\/s00421-005-0070-z","article-title":"Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development","volume":"96","author":"LL Andersen","year":"2006","journal-title":"European journal of applied physiology"},{"issue":"3","key":"pone.0277949.ref028","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1002\/mus.21021","article-title":"Effect of contraction mode of slow-speed resistance training on the maximum rate of force development in the human quadriceps","volume":"38","author":"AJ Blazevich","year":"2008","journal-title":"Muscle Nerve"},{"issue":"5","key":"pone.0277949.ref029","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S1050-6411(00)00027-4","article-title":"Development of recommendations for SEMG sensors and sensor placement procedures","volume":"10","author":"HJ Hermens","year":"2000","journal-title":"J Electromyogr Kinesiol"},{"issue":"5","key":"pone.0277949.ref030","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/S1050-6411(02)00033-0","article-title":"EMG-angle relationship of the hamstring muscles during maximum knee flexion","volume":"12","author":"H Onishi","year":"2002","journal-title":"J Electromyogr Kinesiol"},{"issue":"6","key":"pone.0277949.ref031","doi-asserted-by":"crossref","first-page":"1406","DOI":"10.1016\/j.jelekin.2013.08.009","article-title":"Knee joint angle affects EMG-force relationship in the vastus intermedius muscle","volume":"23","author":"A Saito","year":"2013","journal-title":"J Electromyogr Kinesiol"},{"issue":"469","key":"pone.0277949.ref032","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1198\/016214504000001907","article-title":"Daniel False Discovery Rate: Adjusted Multiple Confidence Intervals for Selected Parameters","volume":"100","author":"YY Benjamini","year":"2005","journal-title":"Journal of the American Statistical Association"},{"key":"pone.0277949.ref033","first-page":"567","volume-title":"Statistical power analysis for the behavioral sciences","author":"J. Cohen","year":"1988","edition":"2"},{"issue":"5","key":"pone.0277949.ref034","doi-asserted-by":"crossref","first-page":"354","DOI":"10.2519\/jospt.2011.3268","article-title":"Selective strength loss and decreased muscle activity in hamstring injury","volume":"41","author":"G Sole","year":"2011","journal-title":"The Journal of orthopaedic and sports physical therapy"},{"issue":"2","key":"pone.0277949.ref035","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1113\/jphysiol.1973.sp010192","article-title":"The orderly recruitment of human motor units during voluntary isometric contractions","volume":"230","author":"HS Milner-Brown","year":"1973","journal-title":"The Journal of physiology"},{"issue":"2","key":"pone.0277949.ref036","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1097\/00003677-200304000-00002","article-title":"Training-induced changes in neural function.","volume":"31","author":"P. Aagaard","year":"2003","journal-title":"Exerc Sport Sci Rev"},{"issue":"3","key":"pone.0277949.ref037","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1007\/BF00690890","article-title":"Motor unit activity and surface electromyogram power spectrum during increasing force of contraction","volume":"56","author":"T Moritani","year":"1987","journal-title":"Eur J Appl Physiol Occup Physiol"},{"issue":"4","key":"pone.0277949.ref038","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1007\/BF02350984","article-title":"Methods for estimating muscle fibre conduction velocity from surface electromyographic signals","volume":"42","author":"D Farina","year":"2004","journal-title":"Med Biol Eng Comput"},{"issue":"1","key":"pone.0277949.ref039","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/1050-6411(92)90004-3","article-title":"The median frequency of the surface EMG power spectrum in relation to motor unit firing and action potential properties","volume":"2","author":"HJ Hermens","year":"1992","journal-title":"J Electromyogr Kinesiol"},{"issue":"4","key":"pone.0277949.ref040","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1097\/00005768-200004000-00015","article-title":"Decreased EMG median frequency during a second bout of eccentric contractions.","volume":"32","author":"GL Warren","year":"2000","journal-title":"Med Sci Sports Exerc"},{"issue":"1","key":"pone.0277949.ref041","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1152\/jn.00084.2018","article-title":"Muscle coactivation: definitions, mechanisms, and functions","volume":"120","author":"ML Latash","year":"2018","journal-title":"J Neurophysiol"},{"issue":"3","key":"pone.0277949.ref042","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1152\/jappl.1992.73.3.911","article-title":"Adaptations in coactivation after isometric resistance training","volume":"73","author":"B Carolan","year":"1992","journal-title":"Journal of applied physiology (Bethesda, Md: 1985)."},{"issue":"1","key":"pone.0277949.ref043","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1111\/j.1600-0838.2005.00441.x","article-title":"Predictors of hamstring injury at the elite level of Australian football","volume":"16","author":"BJ Gabbe","year":"2006","journal-title":"Scand J Med Sci Sports"},{"issue":"no. 3","key":"pone.0277949.ref044","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3233\/IES-2000-0048","article-title":"Jean-Michela. Hamstring muscle tear with recurrent complaints: An isokinetic profile","volume":"8","author":"J-LC Croisier","year":"2000","journal-title":"sokinetics and Exercise Science"},{"issue":"5","key":"pone.0277949.ref045","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1177\/036354658701500504","article-title":"Biomechanical comparison of stimulated and nonstimulated skeletal muscle pulled to failure","volume":"15","author":"WE Garrett","year":"1987","journal-title":"Am J Sports Med"},{"issue":"3","key":"pone.0277949.ref046","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1152\/jappl.1996.80.3.765","article-title":"Adaptive responses to muscle lengthening and shortening in humans","volume":"80","author":"T Hortobagyi","year":"1996","journal-title":"Journal of applied physiology (Bethesda, Md: 1985)."}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0277949","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T20:11:46Z","timestamp":1669925506000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0277949"}},"subtitle":[],"editor":[{"given":"Sumiaki","family":"Maeo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,12,1]]},"references-count":46,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12,1]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0277949","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,1]]}}}