{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,2]],"date-time":"2026-04-02T18:52:05Z","timestamp":1775155925449,"version":"3.50.1"},"reference-count":50,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2024,6,20]],"date-time":"2024-06-20T00:00:00Z","timestamp":1718841600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"MINISTERO DELLA DIFESA","award":["M_D E13985 REG2021 0032116 28-07-2021 (Project AMAMP)"],"award-info":[{"award-number":["M_D E13985 REG2021 0032116 28-07-2021 (Project AMAMP)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JFMK"],"abstract":"<jats:p>This study aimed to compare neuromuscular fatigability of the elbow flexors and extensors between athletes with amputation (AMP) and athletes with spinal cord injury (SCI) for maximum voluntary force (MVF) and rate of force development (RFD). We recruited 20 para-athletes among those participating at two training camps (2022) for Italian Paralympic veterans. Ten athletes with SCI (two with tetraplegia and eight with paraplegia) were compared to 10 athletes with amputation (above the knee, N = 3; below the knee, N = 6; forearm, N = 1). We quantified MVF, RFD at 50, 100, and 150 ms, and maximal RFD (RFDpeak) of elbow flexors and extensors before and after an incremental arm cranking to voluntary fatigue. We also measured the RFD scaling factor (RFD-SF), which is the linear relationship between peak force and peak RFD quantified in a series of ballistic contractions of submaximal amplitude. SCI showed lower levels of MVF and RFD in both muscle groups (all p values \u2264 0.045). Despite this, the decrease in MVF (Cohen\u2019s d = 0.425, p &lt; 0.001) and RFDpeak (d = 0.424, p = 0.003) after the incremental test did not show any difference between pathological conditions. Overall, RFD at 50 ms showed the greatest decrease (d = 0.741, p &lt; 0.001), RFD at 100 ms showed a small decrease (d = 0.382, p = 0.020), and RFD at 150 ms did not decrease (p = 0.272). The RFD-SF decreased more in SCI than AMP (p &lt; 0.0001). Muscle fatigability impacted not only maximal force expressions but also the quickness of ballistic contractions of submaximal amplitude, particularly in SCI. This may affect various sports and daily living activities of wheelchair users. Early RFD (i.e., \u226450 ms) was notably affected by muscle fatigability.<\/jats:p>","DOI":"10.3390\/jfmk9020108","type":"journal-article","created":{"date-parts":[[2024,6,21]],"date-time":"2024-06-21T03:44:49Z","timestamp":1718941489000},"page":"108","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Upper-Limb Muscle Fatigability in Para-Athletes Quantified as the Rate of Force Development in Rapid Contractions of Submaximal Amplitude"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8706-4098","authenticated-orcid":false,"given":"Gennaro","family":"Boccia","sequence":"first","affiliation":[{"name":"Department of Clinical and Biological Sciences, University of Turin, 10043 Turin, Italy"},{"name":"Neuromuscular Function Research Group, School of Exercise and Sport Science, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8422-5132","authenticated-orcid":false,"given":"Paolo Riccardo","family":"Brustio","sequence":"additional","affiliation":[{"name":"Department of Clinical and Biological Sciences, University of Turin, 10043 Turin, Italy"},{"name":"Neuromuscular Function Research Group, School of Exercise and Sport Science, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8479-0067","authenticated-orcid":false,"given":"Luca","family":"Beratto","sequence":"additional","affiliation":[{"name":"Neuromuscular Function Research Group, School of Exercise and Sport Science, University of Turin, 10126 Turin, Italy"},{"name":"Department of Medical Sciences, University of Turin, 10126 Turin, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6210-5241","authenticated-orcid":false,"given":"Ilaria","family":"Peluso","sequence":"additional","affiliation":[{"name":"Research Centre for Food and Nutrition (CREA-AN), 00178 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-2810-6162","authenticated-orcid":false,"given":"Roberto","family":"Ferrara","sequence":"additional","affiliation":[{"name":"Rehabilitation Medicine Department, Italian Army Medical Hospital, 00143 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9446-8277","authenticated-orcid":false,"given":"Diego","family":"Munzi","sequence":"additional","affiliation":[{"name":"Joint Veteran Defence Center, 00184 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3798-7745","authenticated-orcid":false,"given":"Elisabetta","family":"Toti","sequence":"additional","affiliation":[{"name":"Research Centre for Food and Nutrition (CREA-AN), 00178 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4021-6829","authenticated-orcid":false,"given":"Anna","family":"Raguzzini","sequence":"additional","affiliation":[{"name":"Research Centre for Food and Nutrition (CREA-AN), 00178 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1187-1242","authenticated-orcid":false,"given":"Tommaso","family":"Sciarra","sequence":"additional","affiliation":[{"name":"Rehabilitation Medicine Department, Italian Army Medical Hospital, 00143 Rome, Italy"},{"name":"Joint Veteran Defence Center, 00184 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4553-2898","authenticated-orcid":false,"given":"Alberto","family":"Rainoldi","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, University of Turin, 10126 Turin, Italy"},{"name":"Research Centre for Food and Nutrition (CREA-AN), 00178 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1038\/s41393-020-0470-2","article-title":"Wheelchair propulsion fatigue thresholds in electromyographic and ventilatory testing","volume":"58","author":"Qi","year":"2020","journal-title":"Spinal Cord"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1016\/j.medengphy.2005.12.001","article-title":"Manual wheelchairs: Research and innovation in rehabilitation, sports, daily life and health","volume":"28","author":"Janssen","year":"2006","journal-title":"Med. Eng. Phys."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1682\/JRRD.2003.01.0027","article-title":"Upper-limb fatigue-related joint power shifts in experienced wheelchair users and nonwheelchair users","volume":"40","author":"Rodgers","year":"2003","journal-title":"J. Rehabil. Res. Dev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.1152\/physrev.2001.81.4.1725","article-title":"Spinal and supraspinal factors in human muscle fatigue","volume":"81","author":"Gandevia","year":"2001","journal-title":"Physiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1007\/s00421-016-3346-6","article-title":"Rate of force development: Physiological and methodological considerations","volume":"116","author":"Maffiuletti","year":"2016","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_6","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":"Aagaard","year":"2018","journal-title":"Clin. Physiol. Funct. Imaging"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1249\/MSS.0b013e3181be9c7e","article-title":"Neuromuscular performance of explosive power athletes versus untrained individuals","volume":"42","author":"Tillin","year":"2010","journal-title":"Med. Sci. Sports. Exerc."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1519\/JSC.0b013e3181be305c","article-title":"The role of rate of force development on vertical jump performance","volume":"25","author":"McLellan","year":"2011","journal-title":"J. Strength Cond. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1113\/jphysiol.2007.135392","article-title":"Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men","volume":"583","author":"Maganaris","year":"2007","journal-title":"J. Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"538","DOI":"10.2522\/ptj.20090167","article-title":"Muscle activation and perceived loading during rehabilitation exercises: Comparison of dumbbells and elastic resistance","volume":"90","author":"Andersen","year":"2010","journal-title":"Phys. Ther."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"772","DOI":"10.2519\/jospt.2012.3780","article-title":"Rate of Force Development as an Adjunctive Outcome Measure for Return-to-Sport Decisions After Anterior Cruciate Ligament Reconstruction","volume":"42","author":"Angelozzi","year":"2012","journal-title":"J. Orthop. Sports Phys."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1113\/expphysiol.2013.075614","article-title":"Central fatigue contributes to the greater reductions in explosive than maximal strength with high-intensity fatigue","volume":"99","author":"Buckthorpe","year":"2014","journal-title":"Exp. Physiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1111\/sms.12241","article-title":"Rate of force development as a measure of muscle damage","volume":"25","author":"Blazevich","year":"2015","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2065","DOI":"10.1007\/s00421-019-04195-6","article-title":"Experimental knee pain impairs joint torque and rate of force development in isometric and isokinetic muscle activation","volume":"119","author":"Rice","year":"2019","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1249\/JES.0000000000000306","article-title":"Neuromechanics of the Rate of Force Development","volume":"51","year":"2023","journal-title":"Exerc. Sport Sci. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"701916","DOI":"10.3389\/fnhum.2021.701916","article-title":"Rate of Force Development as an Indicator of Neuromuscular Fatigue: A Scoping Review","volume":"15","author":"Maffiuletti","year":"2021","journal-title":"Front. Hum. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e14528","DOI":"10.1111\/sms.14528","article-title":"Decreased neural drive affects the early rate of force development after repeated burst-like isometric contractions","volume":"34","author":"Boccia","year":"2024","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1111\/sms.14244","article-title":"Neural and contractile determinants of burst-like explosive isometric contractions of the knee extensors","volume":"33","author":"Tarperi","year":"2023","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"102486","DOI":"10.1016\/j.jelekin.2020.102486","article-title":"Early vs. late rate of torque development: Relation with maximal strength and influencing factors","volume":"55","author":"Cossich","year":"2020","journal-title":"J. Electromyogr. Kinesiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/s00221-011-2735-7","article-title":"The rate of force development scaling factor (RFD-SF): Protocol, reliability, and muscle comparisons","volume":"212","author":"Bellumori","year":"2011","journal-title":"Exp. Brain Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"025002","DOI":"10.1088\/1361-6579\/aaff24","article-title":"Relevance of evaluating the rate of torque development in ballistic contractions of submaximal amplitude","volume":"40","author":"Brustio","year":"2019","journal-title":"Physiol. Meas."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1002\/mus.24229","article-title":"Assessment of the rate of force development scaling factor for the hip muscles","volume":"50","author":"Casartelli","year":"2014","journal-title":"Muscle Nerve"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"015001","DOI":"10.1088\/1361-6579\/aa9f51","article-title":"Methodological considerations in the calculation of the rate of force development scaling factor","volume":"39","author":"Djordjevic","year":"2017","journal-title":"Physiol. Meas."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF00235800","article-title":"The relationship between speed and amplitude of the fastest voluntary contractions of human arm muscles","volume":"31","author":"Freund","year":"1978","journal-title":"Exp. Brain Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1152\/japplphysiol.00550.2007","article-title":"Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions","volume":"104","author":"Klass","year":"2008","journal-title":"J. Appl. Physiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1136\/jnnp.54.3.210","article-title":"Abnormal most-rapid isometric contractions in patients with Parkinson\u2019s disease","volume":"54","author":"Wierzbicka","year":"1991","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1152\/jn.00767.2005","article-title":"Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds","volume":"95","author":"Ivanenko","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1152\/jn.00727.2010","article-title":"Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients","volume":"106","author":"Gizzi","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1123\/mcj.17.4.370","article-title":"Age-related decline in the rate of force development scaling factor","volume":"17","author":"Bellumori","year":"2013","journal-title":"Motor Control"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1123\/mc.2019-0021","article-title":"Age-and Sex-Related Differences in the Maximum Muscle Performance and Rate of Force Development Scaling Factor of Precision Grip Muscles","volume":"24","author":"Donato","year":"2020","journal-title":"Motor Control"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"29","DOI":"10.5114\/jhk\/182889","article-title":"Unique Neural Mechanisms Underlying Speed Control of Low-Force Ballistic Contractions","volume":"90","author":"Kim","year":"2024","journal-title":"J. Hum. Kinet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.3389\/fphys.2018.01503","article-title":"Neuromuscular Fatigue Does Not Impair the Rate of Force Development in Ballistic Contractions of Submaximal Amplitudes","volume":"9","author":"Boccia","year":"2018","journal-title":"Front. Physiol."},{"key":"ref_33","first-page":"38","article-title":"Dietary intakes and food habits of wheelchair basketball athletes compared to gym attendees and individuals who do not practice sport activity","volume":"22","author":"Toti","year":"2022","journal-title":"Endocr. Metab. Immune Disord.-Drug Targets (Former. Curr. Drug Targets-Immune Endocr. Metab. Disord.)"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Boccia, G., D\u2019Emanuele, S., Brustio, P.R., Beratto, L., Tarperi, C., Casale, R., Sciarra, T., and Rainoldi, A. (2022). Strength Asymmetries Are Muscle-Specific and Metric-Dependent. Int. J. Environ. Res. Public Health, 19.","DOI":"10.3390\/ijerph19148495"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1002\/mus.23934","article-title":"Innervation zone locations in 43 superficial muscles: Toward a standardization of electrode positioning","volume":"49","author":"Rainoldi","year":"2014","journal-title":"Muscle Nerve"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"102363","DOI":"10.1016\/j.jelekin.2019.102363","article-title":"Tutorial. Surface EMG detection in space and time: Best practices","volume":"49","author":"Merletti","year":"2019","journal-title":"J. Electromyogr. Kinesiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3389\/fnhum.2021.654443","article-title":"Advancements in the Protocol for Rate of Force Development\/Relaxation Scaling Factor Evaluation","volume":"15","author":"Smajla","year":"2021","journal-title":"Front. Hum. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"035010","DOI":"10.1088\/1361-6579\/abef56","article-title":"Onset detection in surface electromyographic signals across isometric explosive and ramped contractions: A comparison of computer-based methods","volume":"42","author":"Crotty","year":"2021","journal-title":"Physiol. Meas."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1519\/JSC.0000000000000705","article-title":"A Comparison of Methods for Determining the Rate of Force Development During Isometric Midthigh Clean Pulls","volume":"29","author":"Haff","year":"2015","journal-title":"J. Strength Cond. Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1080\/02640411003642098","article-title":"Effects of age and limb dominance on upper and lower limb muscle function in healthy males and females aged 40\u201380 years","volume":"28","author":"Ditroilo","year":"2010","journal-title":"J. Sport Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1080\/00401706.1977.10489493","article-title":"Detection of influential observation in linear regression","volume":"19","author":"Cook","year":"1977","journal-title":"Technometrics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1007\/s00421-017-3595-z","article-title":"Reliability of quadriceps surface electromyography measurements is improved by two vs. single site recordings","volume":"117","author":"Balshaw","year":"2017","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.humov.2017.05.016","article-title":"Fatigue-induced dissociation between rate of force development and maximal force across repeated rapid contractions","volume":"54","author":"Boccia","year":"2017","journal-title":"Hum. Mov. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1111\/sms.12718","article-title":"Central and peripheral fatigue in knee and elbow extensor muscles after a long-distance cross-country ski race","volume":"27","author":"Boccia","year":"2016","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2445","DOI":"10.1113\/JP277396","article-title":"You are as fast as your motor neurons: Speed of recruitment and maximal discharge of motor neurons determine the maximal rate of force development in humans","volume":"597","author":"Negro","year":"2019","journal-title":"J. Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1007\/s00421-022-04889-4","article-title":"The rate of force development scaling factor: A review of underlying factors, assessment methods and potential for practical applications","volume":"122","author":"Kozinc","year":"2022","journal-title":"Eur. J. Appl. Physiol."},{"key":"ref_47","first-page":"745","article-title":"Inter-Limb Asymmetries in Volleyball Players: Differences between Testing Approaches and Association with Performance","volume":"19","author":"Kozinc","year":"2020","journal-title":"J. Sports Sci. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"871","DOI":"10.3389\/fphys.2021.679322","article-title":"Quantification of inter-limb symmetries with rate of force development and relaxation scaling factor","volume":"12","author":"Smajla","year":"2021","journal-title":"Front. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1249\/MSS.0000000000001069","article-title":"High-Speed Cycling Intervention Improves Rate-Dependent Mobility in Older Adults","volume":"49","author":"Bellumori","year":"2017","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"103817","DOI":"10.1016\/j.msard.2022.103817","article-title":"Isometric tests to evaluate upper and lower extremity functioning in people with multiple sclerosis: Reliability and validity","volume":"63","author":"Uygur","year":"2022","journal-title":"Mult. Scler. Relat. Disord."}],"container-title":["Journal of Functional Morphology and Kinesiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2411-5142\/9\/2\/108\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:02:04Z","timestamp":1760108524000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2411-5142\/9\/2\/108"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,20]]},"references-count":50,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["jfmk9020108"],"URL":"https:\/\/doi.org\/10.3390\/jfmk9020108","relation":{},"ISSN":["2411-5142"],"issn-type":[{"value":"2411-5142","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,20]]}}}