Top

Published in:

01-01-2020 | Electromyographic | Invited Review

Peripheral fatigue: new mechanistic insights from recent technologies

Authors: Emiliano Cè, Stefano Longo, Eloisa Limonta, Giuseppe Coratella, Susanna Rampichini, Fabio Esposito

Published in: European Journal of Applied Physiology | Issue 1/2020

Abstract

Peripheral fatigue results from multiple electrochemical and mechanical events in the cell body and the muscle–tendon complex. Combined force and surface electromyographic signal analysis is among the most widely used approaches to describe the behaviour of a fatigued muscle. Advances in technologies and methodological procedures (e.g. laser diffraction, ³¹P magnetic resonance spectroscopy, shear-wave elastography, tensiomyography, myotonometry, mechanomyography, and high-density surface electromyography) have expanded our knowledge of muscle behaviour before, during, and after a fatiguing task. This review gives an update on recent developments in technologies for investigating the effects of peripheral fatigue linked to skeletal muscle contraction and on mechanistic insights into the electrochemical and mechanical aspects of fatigue. The salient points from the literature analysis are: (1) the electrochemical and mechanical events in the cell (alterations in cross-bridge formation and function and in depolarization of the tubular membrane) precede the events taking place at the muscle–tendon complex (decrease in muscle–tendon unit stiffness); (2) the changes in the fatigued muscle are not homogenous along its length and width but rather reflect a functional compartmentalisation that counteracts the decline in performance; (3) fatigue induces changes in load sharing among adjacent/synergistic muscles. A focus of future studies is to observe how these regional differences occur within single muscle fibres. To do this, a combination of different approaches may yield new insights into the mechanisms underlying muscle fatigue and how the muscle counteracts fatigue.

Abboud J, Nougarou F, Pagé I, Cantin V, Massicotte D, Descarreaux M (2014) Trunk motor variability in patients with non-specific chronic low back pain. Eur J Appl Physiol 114:2645–2654. https://doi.org/10.1007/s00421-014-2985-8 CrossRefPubMed

Abboud J, Nougarou F, Lardon A, Dugas C, Descarreaux M (2016) Influence of lumbar muscle fatigue on trunk adaptations during sudden external perturbations. Front Hum Neurosci 10:1–16. https://doi.org/10.3389/fnhum.2016.00576 CrossRef

Aird L, Samuel D, Stokes M (2012) Quadriceps muscle tone, elasticity and stiffness in older males: reliability and symmetry using the MyotonPRO. Arch Gerontol Geriatr 55:e31–e39. https://doi.org/10.1016/j.archger.2012.03.005 CrossRefPubMed

Akagi R, Fukui T, Kubota M, Nakamura M, Ema R (2017) Muscle shear moduli changes and frequency of alternate muscle activity of plantar flexor synergists induced by prolonged low-level contraction. Front Physiol 8:708. https://doi.org/10.3389/fphys.2017.00708 CrossRefPubMedPubMedCentral

Allen DG, Westerblad H (2001) Role of phosphate and calcium stores in muscle fatigue. J Physiol 536:657–665CrossRefPubMedPubMedCentral

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

Al-Zahrani E, Gunasekaran C, Callaghan M, Gaydecki P, Benitez D, Oldham J (2009) Within-day and between-days reliability of quadriceps isometric muscle fatigue using mechanomyography on healthy subjects. J Electromyogr Kinesiol 19:695–703. https://doi.org/10.1016/j.jelekin.2007.12.007 CrossRefPubMed

Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586:161–173. https://doi.org/10.1113/jphysiol.2007.141838 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 11:1–21. https://doi.org/10.2146/ajhp180163 CrossRef

Asmussen E (1979) Muscle fatigue. Med Sci Sports 11:313–321PubMed

Baskin RJ, Roos KP, Yeh Y (1979) Light diffraction study of single skeletal muscle fibres. Biophys J 28:45–64. https://doi.org/10.1016/S0006-3495(79)85158-9 CrossRefPubMedPubMedCentral

Baskin R, Lieber R, Oba T, Yeh Y (1981) Intensity of light diffraction from striated muscle as a function of incident angle. Biophys J 36:759–773. https://doi.org/10.1016/S0006-3495(81)84764-9 CrossRefPubMedPubMedCentral

Beck TW, Housh TJ, Johnson GO, Weir JP, Cramer JT, Coburn JW, Malek MH (2004) Mechanomyographic and electromyographic time and frequency domain responses during submaximal to maximal isokinetic muscle actions of the biceps brachii. Eur J Appl Physiol 92:352–359. https://doi.org/10.1007/s00421-004-1110-9 CrossRefPubMed

Beck TW, Housh TJ, Fry AC, Cramer JT, Weir JP, Schilling BK, Falvo MJ, Moore CA (2007) The influence of muscle fiber type composition on the patterns of responses for electromyographic and mechanomyographic amplitude and mean power frequency during a fatiguing submaximal isometric muscle action. Electromyogr Clin Neurophysiol 47:221–232PubMed

Beck TW, Housh T, Fry AC, Cramer JT, Weir J, Schilling B, Falvo M, Moore C (2009) MMG-EMG cross spectrum and muscle fiber type. Int J Sports Med 30:538–544. https://doi.org/10.1055/s-0029-1202349 CrossRefPubMed

Bendahan D, Giannesini B, Cozzone PJ (2004) Functional investigations of exercising muscle: a noninvasive magnetic resonance spectroscopy-magnetic resonance imaging approach. Cell Mol Life Sci 61:1001–1015. https://doi.org/10.1007/s00018-004-3345-3 CrossRefPubMed

Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 51:396–409CrossRefPubMed

Bigland-Ritchie B (1979) Factors contributing to quantitative surface electromyographic recording and how they are affected by fatigue. Am Rev Respir Dis 119:95–97. https://doi.org/10.1164/arrd.1979.119.2P2.95 CrossRefPubMed

Bizzini M, Mannion AF (2003) Reliability of a new, hand-held device for assessing skeletal muscle stiffness. Clin Biomech 18:459–461. https://doi.org/10.1016/S0268-0033(03)00042-1 CrossRef

Blangsted AK, Sjøgaard G, Madeleine P, Olsen HB, Søgaard K (2005) Voluntary low-force contraction elicits prolonged low-frequency fatigue and changes in surface electromyography and mechanomyography. J Electromyogr Kinesiol 15:138–148. https://doi.org/10.1016/j.jelekin.2004.10.004 CrossRefPubMed

Bouillard K, Hug F, Guevel A, Nordez A (2012) Shear elastic modulus can be used to estimate an index of individual muscle force during a submaximal isometric fatiguing contraction. J Appl Physiol 113:1353–1361. https://doi.org/10.1152/japplphysiol.00858.2012 CrossRefPubMed

Bouillard K, Jubeau M, Nordez A, Hug F (2014) Effect of vastus lateralis fatigue on load sharing between quadriceps femoris muscles during isometric knee extensions. J Neurophysiol 111:768–776. https://doi.org/10.1152/jn.00595.2013 CrossRefPubMed

Bull AJ, Housh TJ, Johnson GO, Perry SR (2000) Electromyographic and mechanomyographic responses at critical power. Can J Appl Physiol 25:262–270. https://doi.org/10.1139/h00-020 CrossRefPubMed

Cady EB, Elshove H, Jones DA, Moll A (1989a) The metabolic causes of slow relaxation in fatigued human skeletal muscle. J Physiol 418:327–337. https://doi.org/10.1113/jphysiol.1989.sp017843 CrossRefPubMedPubMedCentral

Cady EB, Jones DA, Lynn J, Newham DJ (1989b) Changes in force and intracellular metabolites during fatigue of human skeletal muscle. J Physiol 418:311–325CrossRefPubMedPubMedCentral

Camic CL, Housh TJ, Zuniga JM, Russell Hendrix C, Bergstrom HC, Traylor DA, Schmidt RJ, Johnson GO (2013) Electromyographic and mechanomyographic responses across repeated maximal isometric and concentric muscle actions of the leg extensors. J Electromyogr Kinesiol 23:342–348. https://doi.org/10.1016/j.jelekin.2012.09.010 CrossRefPubMed

Camic CL, Housh TJ, Zuniga JM, Bergstrom HC, Schmidt RJ, Johnson GO (2014) Mechanomyographic and electromyographic responses during fatiguing eccentric muscle actions of the leg extensors. J Appl Biomech 30:255–261. https://doi.org/10.1123/jab.2013-0178 CrossRefPubMed

Carrasco L, Sañudo B, De Hoyo M, Pradas F, Da Silva ME (2011) Effectiveness of low-frequency vibration recovery method on blood lactate removal, muscle contractile properties and on time to exhaustion during cycling at VO₂max power output. Eur J Appl Physiol 111:2271–2279. https://doi.org/10.1007/s00421-011-1848-9 CrossRefPubMed

Cavanagh PR, Komi PV (1979) Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol 42:159–163CrossRefPubMed

Cè E, Rampichini S, Agnello L, Limonta E, Veicsteinas A, Esposito F (2013) Effects of temperature and fatigue on the electromechanical delay components. Muscle Nerve 47:566–576. https://doi.org/10.1002/mus.23627 CrossRefPubMed

Cè E, Rampichini S, Limonta E, Esposito F (2014) Fatigue effects on the electromechanical delay components during the relaxation phase after isometric contraction. Acta Physiol 211:82–96. https://doi.org/10.1111/apha.12212 CrossRef

Cè E, Rampichini S, Esposito F (2015a) Novel insights into skeletal muscle function by mechanomyography: from the laboratory to the field. Sport Sci Health 11:1–28. https://doi.org/10.1007/s11332-015-0219-z CrossRef

Cè E, Rampichini S, Venturelli M, Limonta E, Veicsteinas A, Esposito F (2015b) Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51:907–915. https://doi.org/10.1002/mus.24466 CrossRefPubMed

Cè E, Rampichini S, Monti E, Venturelli M, Limonta E, Esposito F (2017) Changes in the electromechanical delay components during a fatiguing stimulation in human skeletal muscle: an EMG, MMG and force combined approach. Eur J Appl Physiol 117:95–107. https://doi.org/10.1007/s00421-016-3502-z CrossRefPubMed

Curtin NA, Edman KAP (1989) Effects of fatigue and reduced intracellular pH on segment dynamics in “isometric” relaxation of frog muscle fibres. J Physiol 413:159–174CrossRefPubMedPubMedCentral

Dahmane R, Valenčič V, Knez N, Eržen I (2001) Evaluation of the ability to make non-invasive estimation of muscle contractile properties on the basis of the muscle belly response. Med Biol Eng Comput 39:51–55. https://doi.org/10.1007/BF02345266 CrossRefPubMed

Dahmane R, Djordjevič S, Šimunič B, Valenčič V (2005) Spatial fiber type distribution in normal human muscle: histochemical and tensiomyographical evaluation. J Biomech 38:2451–2459. https://doi.org/10.1016/j.jbiomech.2004.10.020 CrossRefPubMed

de Paula Simola RÁ, Harms N, Raeder C, Kellmann M, Meyer T, Pfeiffer M, Ferrauti A (2015) Tensiomyography reliability and prediction of changes in muscle force following heavy eccentric strength exercise using muscle mechanical properties. Sport Technol 8:58–66. https://doi.org/10.1080/19346182.2015.1117475 CrossRef

de Paula Simola RÁ, Raeder C, Wiewelhove T, Kellmann M, Meyer T, Pfeiffer M, Ferrauti A (2016) Muscle mechanical properties of strength and endurance athletes and changes after one week of intensive training. J Electromyogr Kinesiol 30:73–80. https://doi.org/10.1016/j.jelekin.2016.05.005 CrossRefPubMed

Debold EP (2006) The depressive effect of Pi on the force-pCa relationship in skinned single muscle fibers is temperature dependent. AJP Cell Physiol 290:C1041–C1050. https://doi.org/10.1152/ajpcell.00342.2005 CrossRef

Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S (2012) Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sport 22:381–391. https://doi.org/10.1111/j.1600-0838.2010.01167.x CrossRef

Degroot M, Massie BM, Boska M, Gober J, Miller RG, Weiner MW (1993) Dissociation of [H+] from fatigue in human muscle detected by high time resolution 31P-NMR. Muscle Nerve 16:91–98. https://doi.org/10.1002/mus.880160115 CrossRefPubMed

Ditroilo M, Hunter AM, Haslam S, De Vito G (2011) The effectiveness of two novel techniques in establishing the mechanical and contractile responses of biceps femoris. Physiol Meas 32:1315–1326. https://doi.org/10.1088/0967-3334/32/8/020 CrossRefPubMed

Ditroilo M, Smith IJ, Fairweather MM, Hunter AM (2013) Long-term stability of tensiomyography measured under different muscle conditions. J Electromyogr Kinesiol 23:558–563. https://doi.org/10.1016/j.jelekin.2013.01.014 CrossRefPubMed

Drost G, Stegeman DF, van Engelen BGM, Zwarts MJ (2006) Clinical applications of high-density surface EMG: a systematic review. J Electromyogr Kinesiol 16:586–602CrossRefPubMed

Ebersole KT, Malek DM (2008) Fatigue and the electromechanical efficiency of the vastus medialis and vastus lateralis muscles. J Athl Train 43:152–156. https://doi.org/10.4085/1062-6050-43.2.152 CrossRefPubMedPubMedCentral

Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46:2381–2387. https://doi.org/10.1016/j.jbiomech.2013.07.033 CrossRefPubMed

Edman KAP (1966) The relation between sarcomere length and active tension in isolated semitendinosus fibres of the frog. J Physiol 183:407–417. https://doi.org/10.1113/jphysiol.1966.sp007873 CrossRefPubMedPubMedCentral

Edman KAP, Flitney FW (1982) Laser diffraction studies of sarcomere dynamics during ‘isometric’ relaxation in isolated muscle fibres of the frog. J Physiol 329:1–20. https://doi.org/10.1113/jphysiol.1982.sp014287 CrossRefPubMedPubMedCentral

Edman KAP, Lou F (1990) Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J Physiol 424:133–149. https://doi.org/10.1113/jphysiol.1990.sp018059 CrossRefPubMedPubMedCentral

Edman KAP, Lou F (1992) Myofibrillar fatigue versus failure of activation during repetitive stimulation of frog muscle fibres. J Physiol 457:655–673CrossRefPubMedPubMedCentral

Edman KAP, Reggiani C, te Kronnie G (1985) Differences in maximum velocity of shortening along single muscle fibres of the frog. J Physiol 365:147–163CrossRefPubMedPubMedCentral

Esposito F, Orizio C, Veicsteinas A (1998) Electromyogram and mechanomyogram changes in fresh and fatigued muscle during sustained contraction in men. Eur J Appl Physiol Occup Physiol 78:494–501. https://doi.org/10.1007/s004210050451 CrossRefPubMed

Esposito F, Orizio C, Parrinello G, Veicsteinas A (2003) Chronic hypobaric hypoxia does not affect electro-mechanical muscle activities during sustained maximal isometric contractions. Eur J Appl Physiol 90:337–343. https://doi.org/10.1007/s00421-003-0922-3 CrossRefPubMed

Esposito F, Limonta E, Cè E (2011) Passive stretching effects on electromechanical delay and time course of recovery in human skeletal muscle: new insights from an electromyographic and mechanomyographic combined approach. Eur J Appl Physiol 111:485–495. https://doi.org/10.1007/s00421-010-1659-4 CrossRefPubMed

Esposito F, Cè E, Rampichini S, Limonta E, Venturelli M, Monti E, Bet L, Fossati B, Meola G (2016) Electromechanical delay components during skeletal muscle contraction and relaxation in patients with myotonic dystrophy type 1. Neuromuscul Disord 26:60–72. https://doi.org/10.1016/j.nmd.2015.09.013 CrossRefPubMed

Esposito F, Cè E, Rampichini S, Monti E, Limonta E, Fossati B, Meola G (2017) Electromechanical delays during a fatiguing exercise and recovery in patients with myotonic dystrophy type 1. Eur J Appl Physiol 117:551–566. https://doi.org/10.1007/s00421-017-3558-4 CrossRefPubMed

Farina D, Leclerc F, Arendt-Nielsen L, Buttelli O, Madeleine P (2008) The change in spatial distribution of upper trapezius muscle activity is correlated to contraction duration. J Electromyogr Kinesiol 18:16–25. https://doi.org/10.1016/j.jelekin.2006.08.005 CrossRefPubMed

Ferris-Hood K, Threlkeld AJ, Horn TS, Shapiro R (1996) Relaxation electromechanical delay of the quadriceps during selected movement velocities. Electromyogr Clin Neurophysiol 36:157–170PubMed

Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94CrossRefPubMed

Fitts RH (2008) The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104:551–558. https://doi.org/10.1152/japplphysiol.01200.2007 CrossRefPubMed

Fitts RH (2016) The role of acidosis in fatigue: pro perspective. Med Sci Sports Exerc 48:2335–2338. https://doi.org/10.1249/MSS.0000000000001043 CrossRefPubMed

Fryer MW, West JM, Stephenson DG (1997) Phosphate transport into the sarcoplasmic reticulum of skinned fibres from rat skeletal muscle. J Muscle Res Cell Motil 18:161–167. https://doi.org/10.1023/A:1018605605757 CrossRefPubMed

Gallina A, Merletti R, Vieira TMM (2011) Are the myoelectric manifestations of fatigue distributed regionally in the human medial gastrocnemius muscle? J Electromyogr Kinesiol 21:929–938. https://doi.org/10.1016/j.jelekin.2011.08.006 CrossRefPubMed

Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789CrossRefPubMed

García-García O, Cancela-Carral JM, Martínez-Trigo R, Serrano-Gómez V (2013) Differences in the contractile properties of the knee extensor and flexor muscles in professional road cyclists during the season. J Strength Cond Res 27:2760–2767. https://doi.org/10.1519/JSC.0b013e31828155cd CrossRefPubMed

García-García O, Cancela-Carral JM, Huelin-Trillo F (2015) Neuromuscular profile of top-level women kayakers assessed through tensiomyography. J Strength Cond Res 29:844–853. https://doi.org/10.1519/JSC.0000000000000702 CrossRefPubMed

García-Manso JM, Rodríguez-Ruiz D, Rodríguez-Matoso D, de Yves S, Sarmiento S, Quiroga M (2011) Assessment of muscle fatigue after an ultra-endurance triathlon using tensiomyography (TMG). J Sports Sci 29:619–625. https://doi.org/10.1080/02640414.2010.548822 CrossRefPubMed

García-Manso JM, Rodríguez-Matoso D, Sarmiento S, de Saa Y, Vaamonde D, Rodríguez-Ruiz D, Da Silva-Grigoletto ME (2012) Effect of high-load and high-volume resistance exercise on the tensiomyographic twitch response of biceps brachii. J Electromyogr Kinesiol 22:612–619. https://doi.org/10.1016/j.jelekin.2012.01.005 CrossRefPubMed

Gennisson JL, Cornu C, Catheline S, Fink M, Portero P (2005) Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 38:1543–1550. https://doi.org/10.1016/j.jbiomech.2004.07.013 CrossRefPubMed

Gennisson JL, Deffieux T, Fink M, Tanter M (2013) Ultrasound elastography: principles and techniques. Diagn Interv Imaging 94:487–495. https://doi.org/10.1016/j.diii.2013.01.022 CrossRefPubMed

Gerdle B, Grönlund C, Karlsson SJ, Holtermann A, Roeleveld K (2010) Altered neuromuscular control mechanisms of the trapezius muscle in fibromyalgia. BMC Musculoskelet Disord 11:42. https://doi.org/10.1186/1471-2474-11-42 CrossRefPubMedPubMedCentral

Giovanelli N, Taboga P, Rejc E, Simunic B, Antonutto G, Lazzer S (2016) Effects of an uphill marathon on running mechanics and lower-limb muscle fatigue. Int J Sports Physiol Perform 11:522–529. https://doi.org/10.1123/ijspp.2014-0602 CrossRefPubMed

Goldenberg M, Yack H, Cerny F, Burton H (1991) Acoustic myography as an indicator of force during sustained contractions of a small hand muscle. J Appl Physiol 70:87–91CrossRefPubMed

Goldman YE (1987) Measurement of sarcomere shortening in skinned fibers from frog muscle by white light diffraction. Biophys J 52:57–68. https://doi.org/10.1016/S0006-3495(87)83188-0 CrossRefPubMedPubMedCentral

Goonetilleke A, Modarres-Sadeghi H, Guiloff RJ (1994) Accuracy, reproducibility, and variability of hand-held dynamometry in motor neuron disease. J Neurol Neurosurg Psychiatry 57:326–332. https://doi.org/10.1136/jnnp.57.3.326 CrossRefPubMedPubMedCentral

Hendrix CR, Housh TJ, Camic CL, Zuniga JM, Johnson GO, Schmidt RJ (2010) Comparing electromyographic and mechanomyographic frequency-based fatigue thresholds to critical torque during isometric forearm flexion. J Neurosci Methods 194:64–72. https://doi.org/10.1016/j.jneumeth.2010.07.006 CrossRefPubMed

Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hägg G (1999) European recommendations for surface electromyography. Roessingh Res Dev. https://doi.org/10.1016/S1050-6411(00)00027-4 CrossRef

Holtermann A, Roeleveld K, Karlsson JS (2005) Inhomogeneities in muscle activation reveal motor unit recruitment. J Electromyogr Kinesiol 15:131–137. https://doi.org/10.1016/j.jelekin.2004.09.003 CrossRefPubMed

Hoult DI, Busby SJW, Gadian DG, Radda GK, Richards RE, Seeley PJ (1974) Observation of tissue metabolites using 31P nuclear magnetic resonance. Nature 252:285–287. https://doi.org/10.1038/252285a0 CrossRefPubMed

Housh TJ, Perry SR, Bull AJ, Johnson GO, Ebersole KT, Housh DJ, de Vries HA (2000) Mechanomyographic and electromyographic responses during submaximal cycle ergometry. Eur J Appl Physiol 83:381–387. https://doi.org/10.1007/s004210000315 CrossRefPubMed

Hu Y, Siu SH, Mak JN, Luk KD (2010) Lumbar muscle electromyographic dynamic topography during flexion-extension. J Electromyogr Kinesiol 20:246–255. https://doi.org/10.1016/j.jelekin.2009.05.002 CrossRefPubMed

Hufschmidt A (1985) Acoustic phenomena in the latent period of skeletal muscle: a simple method for in vivo measurement of the electro-mechanic latency (EML). Pflugers Arch 404:162–165CrossRefPubMed

Hug F, Tucker K, Gennisson JL, Tanter M, Nordez A (2015) Elastography for muscle biomechanics: toward the estimation of individual muscle force. Exerc Sport Sci Rev 43:125–133. https://doi.org/10.1249/JES.0000000000000049 CrossRefPubMed

Hunter AM, Galloway SDR, Smith IJ, Tallent J, Ditroilo M, Fairweather MM, Howatson G (2012) Assessment of eccentric exercise-induced muscle damage of the elbow flexors by tensiomyography. J Electromyogr Kinesiol 22:334–341. https://doi.org/10.1016/j.jelekin.2012.01.009 CrossRefPubMed

Jaskólski A, Andrzejewska R, Marusiak J, Kisiel-Sajewicz K, Jaskólska A (2007) Similar response of agonist and antagonist muscles after eccentric exercise revealed by electromyography and mechanomyography. J Electromyogr Kinesiol 17:568–577. https://doi.org/10.1016/j.jelekin.2006.05.002 CrossRefPubMed

Jordanic M, Rojas-Martínez M, Mañanas MA, Alonso JF (2016) Spatial distribution of HD-EMG improves identification of task and force in patients with incomplete spinal cord injury. J Neuroeng Rehabil 13:41. https://doi.org/10.1186/s12984-016-0151-8 CrossRefPubMedPubMedCentral

Kawai M, Kuntz ID (1973) Optical diffraction studies of muscle fibers. Biophys J 13:857–876. https://doi.org/10.1016/S0006-3495(73)86031-X CrossRefPubMedPubMedCentral

Kawczyński A, Nie H, Jaskólska A, Jaskólski A, Arendt-Nielsen L, Madeleine P (2007) Mechanomyography and electromyography during and after fatiguing shoulder eccentric contractions in males and females. Scand J Med Sci Sport 17:172–179. https://doi.org/10.1111/j.1600-0838.2006.00551.x CrossRef

Kelly JP, Koppenhaver SL, Michener LA, Proulx L, Bisagni F, Cleland JA (2018) Characterization of tissue stiffness of the infraspinatus, erector spinae, and gastrocnemius muscle using ultrasound shear wave elastography and superficial mechanical deformation. J Electromyogr Kinesiol 38:73–80. https://doi.org/10.1016/j.jelekin.2017.11.001 CrossRefPubMed

Kent-Braun JA (1999) Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol 80:57–63. https://doi.org/10.1007/s004210050558 CrossRefPubMed

Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823. https://doi.org/10.1152/japplphysiol.00091.2002 CrossRefPubMed

Kent-Braun JA, Fitts RH, Christie A (2012) Skeletal muscle fatigue. Compr Physiol 2:997–1044. https://doi.org/10.1002/cphy.c110029 CrossRefPubMed

Kimura T, Hamada T, Watanabe T, Maeda A, Oya T, Moritani T (2004) Mechanomyographic responses in human biceps brachii and soleus during sustained isometric contraction. Eur J Appl Physiol 92:533–539. https://doi.org/10.1007/s00421-004-1147-9 CrossRefPubMed

Kimura T, Fujibayashi M, Tanaka S, Moritani T (2008) Mechanomyographic responses in quadriceps muscles during fatigue by continuous cycle exercise. Eur J Appl Physiol 104:651–656. https://doi.org/10.1007/s00421-008-0816-5 CrossRefPubMed

Kleine BU, van Dijk JP, Lapatki BG, Zwarts MJ, Stegeman DF (2007) Using two-dimensional spatial information in decomposition of surface EMG signals. J Electromyogr Kinesiol 17:535–548. https://doi.org/10.1016/j.jelekin.2006.05.003 CrossRefPubMed

Koo TK, Guo JY, Cohen JH, Parker KJ (2013) Relationship between shear elastic modulus and passive muscle force: an ex vivo study. J Biomech 46:2053–2059. https://doi.org/10.1016/j.jbiomech.2013.05.016 CrossRefPubMed

Kouzaki M, Shinohara M, Fukunaga T (1999) Non-uniform mechanical activity of quadriceps muscle during fatigue by repeated maximal voluntary contraction in humans. Eur J Appl Physiol Occup Physiol 80:9–15. https://doi.org/10.1007/s004210050551 CrossRefPubMed

Križaj D, Šimunič B, Žagar T (2008) Short-term repeatability of parameters extracted from radial displacement of muscle belly. J Electromyogr Kinesiol 18:645–651. https://doi.org/10.1016/j.jelekin.2007.01.008 CrossRefPubMed

Limonta E, Cè E, Gobbo M, Veicsteinas A, Orizio C, Esposito F (2016) Motor unit activation strategy during a sustained isometric contraction of finger flexor muscles in elite climbers. J Sports Sci 34:133–142. https://doi.org/10.1080/02640414.2015.1035738 CrossRefPubMed

Liu CL, Feng YN, Zhang HQ, Li YP, Zhu Y, Zhang ZJ (2018) Assessing the viscoelastic properties of upper trapezius muscle: intra- and inter-tester reliability and the effect of shoulder elevation. J Electromyogr Kinesiol 43:226–229. https://doi.org/10.1016/j.jelekin.2017.09.007 CrossRefPubMed

Longo S, Cè E, Rampichini S, Devoto M, Limonta E, Esposito F (2014) Mechanomyogram amplitude correlates with human gastrocnemius medialis muscle and tendon stiffness both before and after acute passive stretching. Exp Physiol 99:1359–1369. https://doi.org/10.1113/expphysiol.2014.080366 CrossRefPubMed

Longo S, Devoto M, Monti E, Venturelli M, Limonta E, Rampichini S, Valentina A (2016) Acute effects of static stretching on skeletal muscle relaxation at different ankle joint angles. Sport Sci Health 12:429–436. https://doi.org/10.1007/s11332-016-0309-6 CrossRef

Longo S, Cè E, Rampichini S, Devoto M, Venturelli M, Limonta E, Esposito F (2017) Correlation between stiffness and electromechanical delay components during muscle contraction and relaxation before and after static stretching. J Electromyogr Kinesiol 33:83–93. https://doi.org/10.1016/j.jelekin.2017.02.001 CrossRefPubMed

Macgregor LJ, Ditroilo M, Smith IJ, Fairweather MM, Hunter AM (2016) Reduced radial displacement of the gastrocnemius medialis muscle after electrically elicited fatigue. J Sport Rehabil 25:241–247. https://doi.org/10.1123/jsr.2014-0325 CrossRefPubMed

Macgregor LJ, Hunter AM, Orizio C, Fairweather MM, Ditroilo M (2018) Assessment of skeletal muscle contractile properties by radial displacement: the case for tensiomyography. Sport Med 48:1607–1620CrossRef

MacIntosh BR (2017) Recent developments in understanding the length dependence of contractile response of skeletal muscle. Eur J Appl Physiol 117:1059–1071. https://doi.org/10.1007/s00421-017-3591-3 CrossRefPubMed

Madeleine P (2010) On functional motor adaptations: from the quantification of motor strategies to the prevention of musculoskeletal disorders in the neck-shoulder region. Acta Physiol 199:1–46. https://doi.org/10.1111/j.1748-1716.2010.02145.x CrossRef

Madeleine P, Farina D (2008) Time to task failure in shoulder elevation is associated to increase in amplitude and to spatial heterogeneity of upper trapezius mechanomyographic signals. Eur J Appl Physiol 102:325–333. https://doi.org/10.1007/s00421-007-0589-2 CrossRefPubMed

Madeleine P, Farina D, Merletti R, Arendt-Nielsen L (2002a) Upper trapezius muscle mechanomyographic and electromyographic activity in humans during low force fatiguing and non-fatiguing contractions. Eur J Appl Physiol 87:327–336. https://doi.org/10.1007/s00421-002-0655-8 CrossRefPubMed

Madeleine P, Jørgensen LV, Søgaard K, Arendt-Nielsen L, Sjøgaard G (2002b) Development of muscle fatigue as assessed by electromyography and mechanomyography during continuous and intermittent low-force contractions: effects of the feedback mode. Eur J Appl Physiol 87:28–37. https://doi.org/10.1007/s00421-002-0578-4 CrossRefPubMed

Madeleine P, Ge HY, Jaskólska A, Farina D, Jaskölski A, Arendt-Nielsen L (2006) Spectral moments of mechanomyographic signals recorded with accelerometer and microphone during sustained fatiguing contractions. Med Biol Eng Comput 44:290–297. https://doi.org/10.1007/s11517-006-0036-2 CrossRefPubMed

Madeleine P, Tuker K, Arendt-Nielsen L, Farina D (2007) Heterogeneous mechanomyographic absolute activation of paraspinal muscles assessed by a two-dimensional array during short and sustained contractions. J Biomech 40:2663–2671. https://doi.org/10.1016/j.jbiomech.2006.12.011 CrossRefPubMed

Maïsetti O, Hug F, Bouillard K, Nordez A (2012) Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging. J Biomech 45:978–984. https://doi.org/10.1016/j.jbiomech.2012.01.009 CrossRefPubMed

Mamaghani NK, Shimomura Y, Iwanaga K, Katsuura T (2002) Mechanomyogram and electromyogram responses of upper limb during sustained isometric fatigue with varying shoulder and elbow postures. J Physiol Anthropol Appl Hum Sci 21:29–43. https://doi.org/10.2114/jpa.21.29 CrossRef

Marusiak J, Jaskólska A, Koszewicz M, Budrewicz S, Jaskólski A (2012) Myometry revealed medication-induced decrease in resting skeletal muscle stiffness in Parkinson’s disease patients. Clin Biomech 27:632–635. https://doi.org/10.1016/j.clinbiomech.2012.02.001 CrossRef

Merletti R, Knaflitz M, De Luca CJ (1990) Myoelectric manifestations of fatigue in voluntary and electrically elicited contractions. J Appl Physiol 69:1810–1820. https://doi.org/10.1152/jappl.1990.69.5.1810 CrossRefPubMed

Merletti R, Farina D, Gazzoni M (2003) The linear electrode array: a useful tool with many applications. J Electromyogr Kinesiol 13:37–47. https://doi.org/10.1016/S1050-6411(02)00082-2 CrossRefPubMed

Merletti R, Holobar A, Farina D (2008) Analysis of motor units with high-density surface electromyography. J Electromyogr Kinesiol 18:879–890. https://doi.org/10.1016/j.jelekin.2008.09.002 CrossRefPubMed

Miller RG, Giannini D, Milner-Brown HS, Layzer RB, Koretsky AP, Hooper D, Weiner MW (1987) Effects of fatiguing exercise on high-energy phosphates, force, and EMG: evidence for three phases of recovery. Muscle Nerve 10:810–821. https://doi.org/10.1002/mus.880100906 CrossRefPubMed

Miller RG, Boska MD, Moussavi RS, Carson PJ, Weiner MW (1988) 31P nuclear magnetic resonance studies of high energy phosphates and pH in human muscle fatigue. Comparison of aerobic and anaerobic exercise. J Clin Investig 81:1190–1196. https://doi.org/10.1172/JCI113434 CrossRefPubMedPubMedCentral

Mista CA, Salomoni SE, Graven-Nielsen T (2014) Spatial reorganisation of muscle activity correlates with change in tangential force variability during isometric contractions. J Electromyogr Kinesiol 24:37–45. https://doi.org/10.1016/j.jelekin.2013.10.014 CrossRefPubMed

Moon RB, Richards JH (1973) Determination of intracellular pH by 31P magnetic resonance. J Biol Chem 248:7276–7278PubMed

Moritani T, Nagata A, Muro M (1982) Electromyographic manifestations of muscular fatigue. Med Sci Sports Exerc 14:198–202PubMed

Nair K, Masi AT, Andonian BJ, Barry AJ, Coates BA, Dougherty J, Schaefer E, Henderson J, Kelly J (2016) Stiffness of resting lumbar myofascia in healthy young subjects quantified using a handheld myotonometer and concurrently with surface electromyography monitoring. J Bodyw Mov Ther 20:388–396. https://doi.org/10.1016/j.jbmt.2015.12.005 CrossRefPubMed

Nelson CR, Debold EP, Fitts RH (2014) Phosphate and acidosis act synergistically to depress peak power in rat muscle fibers. AJP Cell Physiol 307:C939–C950. https://doi.org/10.1152/ajpcell.00206.2014 CrossRef

Nocella M, Colombini B, Benelli G, Cecchi G, Bagni MA, Bruton J (2011) Force decline during fatigue is due to both a decrease in the force per individual cross-bridge and the number of cross-bridges. J Physiol 589:3371–3381. https://doi.org/10.1113/jphysiol.2011.209874 CrossRefPubMedPubMedCentral

Nordez A, Guével A, Casari P, Catheline S, Cornu C (2009) Assessment of muscle hardness changes induced by a submaximal fatiguing isometric contraction. J Electromyogr Kinesiol 19:484–491. https://doi.org/10.1016/j.jelekin.2007.11.005 CrossRefPubMed

Nosek TM, Fender KY, Godt RE (1987) It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science (80-) 236:191–193CrossRef

O’Connor SM, Cheng EJ, Young KW, Ward SR, Lieber RL (2016) Quantification of sarcomere length distribution in whole muscle frozen sections. J Exp Biol 219:1432–1436. https://doi.org/10.1242/jeb.132084 CrossRefPubMedPubMedCentral

Orizio C (1992) Soundmyogram and EMG cross-spectrum during exhausting isometric contractions in humans. J Electromyogr Kinesiol 2:141–149. https://doi.org/10.1016/1050-6411(92)90011-7 CrossRefPubMed

Orizio C (1993) Muscle sound: bases for the introduction of a mechanomyographic signal in muscle studies. Crit Rev Biomed Eng 21:201–243PubMed

Orizio C, Veicsteinas A (1992) Soundmyogram analysis during sustained maximal voluntary contraction in sprinters and long distance runners. Int J Sports Med 13:594–599. https://doi.org/10.1055/s-2007-1024572 CrossRefPubMed

Orizio C, Perini R, Veicsteinas A (1989) Changes of muscular sound during sustained isometric contraction up to exhaustion. J Appl Physiol 66:1593–1598. https://doi.org/10.1152/jappl.1989.66.4.1593 CrossRefPubMed

Orizio C, Gobbo M, Diemont B, Esposito F, Veicsteinas A (2003) The surface mechanomyogram as a tool to describe the influence of fatigue on biceps brachii motor unit activation strategy. Historical basis and novel evidence. Eur J Appl Physiol 90:326–336. https://doi.org/10.1007/s00421-003-0924-1 CrossRefPubMed

Palmer S, Kentish JC (1994) The role of troponin C in modulating the Ca²⁺ sensitivity of mammalian skinned cardiac and skeletal muscle fibres. J Physiol 480(Pt 1):45–60CrossRefPubMedPubMedCentral

Patel TJ, Das R, Fridén J, Lutz GJ, Lieber RL (2004) Sarcomere strain and heterogeneity correlate with injury to frog skeletal muscle fiber bundles. J Appl Physiol 97:1803–1813CrossRefPubMed

Perry-Rana SR, Housh TJ, Johnson GO, Bull AJ, Berning JM, Cramer JT (2002) MMG and EMG responses during fatiguing isokinetic muscle contractions at different velocities. Muscle Nerve 26:367–373. https://doi.org/10.1002/mus.10214 CrossRefPubMed

Petrofsky JS, Phillips CA (1985) Closed-loop control of movement of skeletal muscle. Crit Rev Biomed Eng 13:35–96PubMed

Piitulainen H, Bottas R, Komi P, Linnamo V, Avela J (2010) Impaired action potential conduction at high force levels after eccentric exercise. J Electromyogr Kinesiol 20:879–887. https://doi.org/10.1016/j.jelekin.2009.10.001 CrossRefPubMed

Pišot R, Narici MV, Šimunič B, De Boer M, Seynnes O, Jurdana M, Biolo G, Mekjavič IB (2008) Whole muscle contractile parameters and thickness loss during 35-day bed rest. Eur J Appl Physiol 104:409–414. https://doi.org/10.1007/s00421-008-0698-6 CrossRefPubMed

Place N, Yamada T, Bruton JD, Westerblad H (2010) Muscle fatigue: from observations in humans to underlying mechanisms studied in intact single muscle fibres. Eur J Appl Physiol 110:1–15. https://doi.org/10.1007/s00421-010-1480-0 CrossRefPubMed

Qayyum A (2009) MR spectroscopy of the liver: principles and clinical applications. RadioGraphics 29:1653–1664. https://doi.org/10.1148/rg.296095520 CrossRefPubMed

Rampichini S, Cè E, Limonta E, Esposito F (2014) Effects of fatigue on the electromechanical delay components in gastrocnemius medialis muscle. Eur J Appl Physiol 114:639–651. https://doi.org/10.1007/s00421-013-2790-9 CrossRefPubMed

Rassier DE, Macintosh BR (2002) Potentiation in mouse skeletal muscle. BMC Physiol 8:1–8

Rau G, Disselhorst-Klug C (1997) Principles of high-spatial-resolution surface EMG (HSR-EMG): single motor unit detection and application in the diagnosis of neuromuscular disorders. J Electromyogr Kinesiol 7:233–239. https://doi.org/10.1016/S1050-6411(97)00007-2 CrossRefPubMed

Rico-Sanz J (2003) Progressive decrease of intramyocellular accumulation of H⁺ and Pi in human skeletal muscle during repeated isotonic exercise. AJP Cell Physiol 284:C1490–C1496. https://doi.org/10.1152/ajpcell.00419.2002 CrossRef

Ringheim I, Indahl A, Roeleveld K (2014) Alternating activation is related to fatigue in lumbar muscles during sustained sitting. J Electromyogr Kinesiol 24:380–386. https://doi.org/10.1016/j.jelekin.2014.01.011 CrossRefPubMed

Rodriguez AA, Agre JC, Franke TM, Swiggum ER, Curt JT (1996) Acoustic myography during isometric fatigue in postpolio and control subjects. Muscle Nerve 19:384–387CrossRefPubMed

Roth K, Weiner MW (1991) Determination of cytosolic ADP and AMP concentrations and the free energy of ATP hydrolysis in human muscle and brain tissues with 31P NMR spectroscopy. Magn Reson Med 22:505–511 [Erratum appears in Magn Reson Med 1995;33(2):282] CrossRefPubMed

Sadeghi S, Newman C, Cortes DH (2018) Change in skeletal muscle stiffness after running competition is dependent on both running distance and recovery time: a pilot study. PeerJ 6:e4469. https://doi.org/10.7717/peerj.4469 CrossRefPubMedPubMedCentral

Sahlin K, Ren JM (1989) Relationship of contraction capacity to metabolic changes during recovery from a fatiguing contraction. J Appl Physiol 67:648–654. https://doi.org/10.1152/jappl.1989.67.2.648 CrossRefPubMed

Samani A, Srinivasan D, Mathiassen SE, Madeleine P (2017) Variability in spatio-temporal pattern of trapezius activity and coordination of hand-arm muscles during a sustained repetitive dynamic task. Exp Brain Res 235:389–400. https://doi.org/10.1007/s00221-016-4798-y CrossRefPubMed

Sasaki K, Sasaki T, Ishii N (2011) Acceleration and force reveal different mechanisms of electromechanical delay. Med Sci Sport Exerc 43:1200–1206. https://doi.org/10.1249/MSS.0b013e318209312c CrossRef

Scherrer J, Bourguignon A (1959) Changes in the electromyogram produced by fatigue in man. Am J Phys Med 38:148–158CrossRefPubMed

Shinohara M, Kouzaki M, Yoshihisa T, Fukunaga T (1997) Mechanomyography of the human quadriceps muscle during incremental cycle ergometry. Eur J Appl Physiol Occup Physiol 76:314–319. https://doi.org/10.1007/s004210050254 CrossRefPubMed

Shinohara M, Kouzaki M, Yoshihisa T, Fukunaga T (1998) Mechanomyogram from the different heads of the quadriceps muscle during incremental knee extension. Eur J Appl Physiol Occup Physiol 78:289–295. https://doi.org/10.1007/s004210050422 CrossRefPubMed

Šimunič B (2012) Between-day reliability of a method for non-invasive estimation of muscle composition. J Electromyogr Kinesiol 22:527–530. https://doi.org/10.1016/j.jelekin.2012.04.003 CrossRefPubMed

Šimunič B, Degens H, Rittweger J, Narici M, Mekjavić IB, Pišot R (2011) Noninvasive estimation of myosin heavy chain composition in human skeletal muscle. Med Sci Sport Exerc 43:1619–1625. https://doi.org/10.1249/MSS.0b013e31821522d0 CrossRef

Smith C, Housh T, Jenkins N, Hill E, Cochrane K, Miramonti A, Schmidt R, Johnson G (2016) Combining regression and mean comparisons to identify the time course of changes in neuromuscular responses during the process of fatigue. Physiol Meas 37:1993–2002. https://doi.org/10.1088/0967-3334/37/11/1993 CrossRefPubMed

Smith CM, Housh TJ, Hill EC, Johnson GO, Schmidt RJ (2017a) Changes in electromechanical delay during fatiguing dynamic muscle actions. Muscle Nerve 56:315–320. https://doi.org/10.1002/mus.25502 CrossRefPubMed

Smith CM, Housh TJ, Hill EC, Johnson GO, Schmidt RJ (2017b) Dynamic versus isometric electromechanical delay in non-fatigued and fatigued muscle: a combined electromyographic, mechanomyographic, and force approach. J Electromyogr Kinesiol 33:34–38. https://doi.org/10.1016/j.jelekin.2017.01.008 CrossRefPubMed

Søgaard K, Blangsted AK, Jørgensen LV, Madeleine P, Sjøgaard G (2003) Evidence of long term muscle fatigue following prolonged intermittent contractions based on mechano- and electromyograms. J Electromyogr Kinesiol 13:441–450. https://doi.org/10.1016/S1050-6411(03)00075-0 CrossRefPubMed

Stegeman DF, Zwarts MJ, Anders C, Hashimoto T (2000) Multi-channel surface EMG in clinical neurophysiology. Suppl Clin Neurophysiol 53:155–162CrossRefPubMed

Stock MS, Beck TW, DeFreitas JM, Ye X (2013) Mechanomyographic responses for the biceps brachii are unable to track the declines in peak torque during 25, 50, 75, and 100 fatiguing isokinetic muscle actions. J Appl Biomech 29:769–778CrossRefPubMed

Taylor DJ, Styles P, Matthews PM, Arnold DA, Gadian D, Bore P, Radda GK (1986) Energetics of human muscle: exercise-induced ATP depletion. Magn Reson Imaging 3:44–54

Tonon C, Gramegna LL, Lodi R (2012) Magnetic resonance imaging and spectroscopy in the evaluation of neuromuscular disorders and fatigue. Neuromuscul Disord 22:S187–S191. https://doi.org/10.1016/j.nmd.2012.10.008 CrossRefPubMed

Tous-Fajardo J, Moras G, Rodríguez-Jiménez S, Usach R, Doutres DM, Maffiuletti NA (2010) Inter-rater reliability of muscle contractile property measurements using non-invasive tensiomyography. J Electromyogr Kinesiol 20:761–766. https://doi.org/10.1016/j.jelekin.2010.02.008 CrossRefPubMed

Troiano A, Naddeo F, Sosso E, Camarota G, Merletti R, Mesin L (2008) Assessment of force and fatigue in isometric contractions of the upper trapezius muscle by surface EMG signal and perceived exertion scale. Gait Posture 28:179–186. https://doi.org/10.1016/j.gaitpost.2008.04.002 CrossRefPubMed

Tucker K, Falla D, Graven-Nielsen T, Farina D (2009) Electromyographic mapping of the erector spinae muscle with varying load and during sustained contraction. J Electromyogr Kinesiol 19:373–379. https://doi.org/10.1016/j.jelekin.2007.10.003 CrossRefPubMed

Udaka J, Terui T, Ohtsuki I, Marumo K, Ishiwata S, Kurihara S, Fukuda N (2011) Depressed contractile performance and reduced fatigue resistance in single skinned fibers of soleus muscle after long-term disuse in rats. J Appl Physiol 111:1080–1087. https://doi.org/10.1152/japplphysiol.00330.2011 CrossRefPubMed

Valenčič V, Knez N (1997) Measuring of skeletal muscles’ dynamic properties. Artif Organs 21:240–242. https://doi.org/10.1111/j.1525-1594.1997.tb04658.x CrossRefPubMed

Van Deun B, Hobbelen JSM, Cagnie B, Van Eetvelde B, Van Den Noortgate N, Cambier D (2018) Reproducible measurements of muscle characteristics using the MyotonPRO device: comparison between individuals with and without paratonia. J Geriatr Phys Ther 41:194–203. https://doi.org/10.1519/JPT.0000000000000119 CrossRefPubMed

Vedsted P, Blangsted AK, Søgaard K, Orizio C, Sjøgaard G (2006) Muscle tissue oxygenation, pressure, electrical, and mechanical responses during dynamic and static voluntary contractions. Eur J Appl Physiol 96:165–177. https://doi.org/10.1007/s00421-004-1216-0 CrossRefPubMed

Viir R, Virkus A, Laiho K, Rajaleid K, Selart A, Mikkelson M (2007) Trapezius muscle tone and viscoelastic properties in sitting and supine positions. Scand J Work Environ Heal Suppl 33:76–80

Viitasalo JT, Komi PV (1981) Interrelationships between electromyographic, mechanical, muscle structure and reflex time measurements in man. Acta Physiol Scand 111:97–103CrossRefPubMed

Wang D, De Vito G, Ditroilo M, Delahunt E (2017a) Effect of sex and fatigue on muscle stiffness and musculoarticular stiffness of the knee joint in a young active population. J Sports Sci 35:1582–1591. https://doi.org/10.1080/02640414.2016.1225973 CrossRefPubMed

Wang D, De Vito G, Ditroilo M, Delahunt E (2017b) Different effect of local and general fatigue on knee joint stiffness. Med Sci Sport Exerc 49:173–182. https://doi.org/10.1249/MSS.0000000000001086 CrossRef

Watanabe K, Kouzaki M, Moritani T (2013) Region-specific myoelectric manifestations of fatigue in human rectus femoris muscle. Muscle Nerve 48:226–234. https://doi.org/10.1002/mus.23739 CrossRefPubMed

Westerblad H (2016) Acidosis is not a significant cause of skeletal muscle fatigue. Med Sci Sports Exerc 48:2339–2342. https://doi.org/10.1249/MSS.0000000000001044 CrossRefPubMed

Westerblad H, Allen DG (2003) Cellular mechanisms of skeletal muscle fatigue. Adv Exp Med Biol 538:563–570 (discussion 571) CrossRefPubMed

Wiewelhove T, Raeder C, Simola RADP, Schneider C, Döweling A, Ferrauti A (2017) Tensiomyographic markers are not sensitive for monitoring muscle fatigue in elite youth athletes: a pilot study. Front Physiol 8:1–9. https://doi.org/10.3389/fphys.2017.00406 CrossRef

Wilkie DR (1986) Muscular fatigue: effects of hydrogen ions and inorganic phosphate. Fed Proc 45:2921–2923PubMed

Wilson JR, McCully KK, Mancini DM, Boden B, Chance B (1988) Relationship of muscular fatigue to pH and diprotonated Pi in humans: a 31P-NMR study. J Appl Physiol 64:2333–2339. https://doi.org/10.1152/jappl.1988.64.6.2333 CrossRefPubMed

Xie HB, Zheng YP, Jing-Yi G (2009) Detection of chaos in human fatigue mechanomyography signals. Conf Proc IEEE Eng Med Biol Soc. https://doi.org/10.1109/IEMBS.2009.5333485 CrossRef

Yang ZF, Kumar DK, Arjunan SP (2009) Mechanomyogram for identifying muscle activity and fatigue. Conf Proc IEEE Eng Med Biol Soc. https://doi.org/10.1109/IEMBS.2009.5333666 CrossRefPubMedCentral

Yoshitake Y, Ue H, Miyazaki M, Moritani T (2001) Assessment of lower-back muscle fatigue using electromyography, mechanomyography, and near-infrared spectroscopy. Eur J Appl Physiol 84:174–179. https://doi.org/10.1007/s004210170001 CrossRefPubMed

Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86:1086–1094CrossRefPubMed

Zinder SM, Padua DA (2011) Reliability, validity, and precision of a handheld myometer for assessing in vivo muscle stiffness. J Sport Rehabil. https://doi.org/10.1123/jsr.2010-0051 CrossRefPubMed

Zuniga JM, Housh TJ, Camic CL, Hendrix CR, Schmidt RJ, Mielke M, Johnson GO (2010) A mechanomyographic fatigue threshold test for cycling. Int J Sports Med 31:636–643. https://doi.org/10.1055/s-0030-1255112 CrossRefPubMed

Zwarts MJ, Keidel M (1991) Relationship between electrical and vibratory output of muscle during voluntary contraction and fatigue. Muscle Nerve 14:756–761. https://doi.org/10.1002/mus.880140810 CrossRefPubMed

Zwarts MJ, Stegeman DF (2003) Multichannel surface EMG: basic aspects and clinical utility. Muscle Nerve 28:1–17. https://doi.org/10.1002/mus.10358 CrossRefPubMed

Title: Peripheral fatigue: new mechanistic insights from recent technologies
Authors: Emiliano Cè
Stefano Longo
Eloisa Limonta
Giuseppe Coratella
Susanna Rampichini
Fabio Esposito
Publication date: 01-01-2020
Publisher: Springer Berlin Heidelberg
Keywords: Electromyographic
Fatigue
Laser
Published in: European Journal of Applied Physiology / Issue 1/2020
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-019-04264-w

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Peripheral fatigue: new mechanistic insights from recent technologies

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2020

The impact of acute and chronic exercise on Nrf2 expression in relation to markers of mitochondrial biogenesis in human skeletal muscle

Hyperinsulinaemia and hyperglycaemia promote glucose utilization and storage during low- and high-intensity exercise

Comparison among three different intensities of eccentric contractions of the elbow flexors resulting in the same strength loss at one day post-exercise for changes in indirect muscle damage markers

Acute hyperketonaemia alters T-cell-related cytokine gene expression within stimulated peripheral blood mononuclear cells following prolonged exercise

The energy cost of swimming and its determinants

Oxygen uptake plateau: calculation artifact or physiological reality?