Skip to main content
Top
Published in: European Journal of Applied Physiology 3/2017

01-03-2017 | Original Article

Electromechanical delays during a fatiguing exercise and recovery in patients with myotonic dystrophy type 1

Authors: Fabio Esposito, Emiliano Cè, Susanna Rampichini, Elena Monti, Eloisa Limonta, Barbara Fossati, Giovanni Meola

Published in: European Journal of Applied Physiology | Issue 3/2017

Login to get access

Abstract

Purpose

The partitioning of the electromechanical delay by an electromyographic (EMG), mechanomyographic (MMG) and force combined approach can provide further insight into the electrochemical and mechanical processes involved with skeletal muscle contraction and relaxation. The aim of the study was to monitor by this combined approach the changes in delays’ electrochemical and mechanical components throughout a fatiguing task and during recovery in patients with myotonic dystrophy type 1 (DM1), who present at the skeletal muscle level fibres rearrangement, muscle weakness and myotonia, especially in the distal muscles.

Methods

After assessing maximum voluntary contraction (MVC), 14 male patients with DM1 and 14 healthy controls (HC) performed a fatiguing exercise at 50% MVC until exhaustion. EMG, MMG, and force signals were recorded from tibialis anterior and vastus lateralis muscles. The electromechanical delay during contraction (DelayTOT) and relaxation (R-DelayTOT) components, EMG and MMG root mean square (RMS) and mean frequency (MF) were calculated off-line.

Results

The fatiguing exercise duration was similar in both groups. In patients with DM1, delays components were significantly longer compared to HC, especially in the distal muscle during relaxation. Delays components recovered quickly from the fatiguing exercise in HC than in patients with DM1 in both muscles.

Conclusions

The alterations in delays observed in DM1 during the fatiguing exercise may indicate that also the lengthening of the electrochemical and mechanical processes during contraction and relaxation could play a role in explaining exercise intolerance in this pathology.
Literature
go back to reference Barchi RL (1975) Myotonia. An evaluation of the chloride hypothesis. Arch Neurol 32(3):175–180CrossRef Barchi RL (1975) Myotonia. An evaluation of the chloride hypothesis. Arch Neurol 32(3):175–180CrossRef
go back to reference Birnberger KL, Klepzig M (1979) Influence of extracellular potassium and intracellular pH on myotonia. J Neurol 222(1):23–35CrossRef Birnberger KL, Klepzig M (1979) Influence of extracellular potassium and intracellular pH on myotonia. J Neurol 222(1):23–35CrossRef
go back to reference 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(2):255–261. doi:10.1123/jab.2013-0178 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(2):255–261. doi:10.​1123/​jab.​2013-0178 CrossRefPubMed
go back to reference Cavanagh PR, Komi PV (1979) Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol 42(3):159–163CrossRef Cavanagh PR, Komi PV (1979) Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol 42(3):159–163CrossRef
go back to reference Ce 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(4):566–576. doi:10.1002/mus.23627 CrossRefPubMed Ce 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(4):566–576. doi:10.​1002/​mus.​23627 CrossRefPubMed
go back to reference Ce E, Rampichini S, Limonta E, Esposito F (2014) Fatigue effects on the electromechanical delay components during the relaxation phase after isometric contraction. Acta Physiol (Oxf) 211(1):82–96. doi:10.1111/apha.12212 CrossRef Ce E, Rampichini S, Limonta E, Esposito F (2014) Fatigue effects on the electromechanical delay components during the relaxation phase after isometric contraction. Acta Physiol (Oxf) 211(1):82–96. doi:10.​1111/​apha.​12212 CrossRef
go back to reference Ce E, Rampichini S, Venturelli M, Limonta E, Veicsteinas A, Esposito F (2015) Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51(6):907–915. doi:10.1002/mus.24466 CrossRefPubMed Ce E, Rampichini S, Venturelli M, Limonta E, Veicsteinas A, Esposito F (2015) Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51(6):907–915. doi:10.​1002/​mus.​24466 CrossRefPubMed
go back to reference Ce E, Rampichini S, Monti E, Venturelli M, Limonta E, Esposito F (2016) 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. doi:10.1007/s00421-016-3502-z CrossRefPubMed Ce E, Rampichini S, Monti E, Venturelli M, Limonta E, Esposito F (2016) 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. doi:10.​1007/​s00421-016-3502-z CrossRefPubMed
go back to reference Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum associates, Hillsdale Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum associates, Hillsdale
go back to reference Edwards JN, Cully TR, Shannon TR, Stephenson DG, Launikonis BS (2012) Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy. J Physiol 590(Pt 3):475–492. doi:10.1113/jphysiol.2011.221796 CrossRefPubMed Edwards JN, Cully TR, Shannon TR, Stephenson DG, Launikonis BS (2012) Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy. J Physiol 590(Pt 3):475–492. doi:10.​1113/​jphysiol.​2011.​221796 CrossRefPubMed
go back to reference 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(6):494–501. doi:10.1007/s004210050451 CrossRefPubMed 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(6):494–501. doi:10.​1007/​s004210050451 CrossRefPubMed
go back to reference Esposito F, Limonta E, Ce 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(3):485–495. doi:10.1007/s00421-010-1659-4 CrossRefPubMed Esposito F, Limonta E, Ce 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(3):485–495. doi:10.​1007/​s00421-010-1659-4 CrossRefPubMed
go back to reference Esposito F, Ce 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(1):60–72. doi:10.1016/j.nmd.2015.09.013 CrossRefPubMed Esposito F, Ce 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(1):60–72. doi:10.​1016/​j.​nmd.​2015.​09.​013 CrossRefPubMed
go back to reference Hammaren E, Kjellby-Wendt G, Kowalski J, Lindberg C (2014) Factors of importance for dynamic balance impairment and frequency of falls in individuals with myotonic dystrophy type 1-A cross-sectional study - Including reference values of Timed Up & Go, 10 m walk and step test. Neuromuscul Disord 24(3):207–215. doi:10.1016/j.nmd.2013.12.003 CrossRefPubMed Hammaren E, Kjellby-Wendt G, Kowalski J, Lindberg C (2014) Factors of importance for dynamic balance impairment and frequency of falls in individuals with myotonic dystrophy type 1-A cross-sectional study - Including reference values of Timed Up & Go, 10 m walk and step test. Neuromuscul Disord 24(3):207–215. doi:10.​1016/​j.​nmd.​2013.​12.​003 CrossRefPubMed
go back to reference Hermens H, Freiks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hagg G (1999) Eurpoean Recommendations for Surface Electromyography. RRD, The Nederlands Hermens H, Freiks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hagg G (1999) Eurpoean Recommendations for Surface Electromyography. RRD, The Nederlands
go back to reference Hiba B, Richard N, Hebert LJ, Cote C, Nejjari M, Vial C, Bouhour F, Puymirat J, Janier M (2012) Quantitative assessment of skeletal muscle degeneration in patients with myotonic dystrophy type 1 using MRI. J Magn Reson Imaging 35(3):678–685. doi:10.1002/jmri.22849 CrossRefPubMed Hiba B, Richard N, Hebert LJ, Cote C, Nejjari M, Vial C, Bouhour F, Puymirat J, Janier M (2012) Quantitative assessment of skeletal muscle degeneration in patients with myotonic dystrophy type 1 using MRI. J Magn Reson Imaging 35(3):678–685. doi:10.​1002/​jmri.​22849 CrossRefPubMed
go back to reference 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). Eur J Physiol 404(2):162–165CrossRef 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). Eur J Physiol 404(2):162–165CrossRef
go back to reference Jaskolski A, Andrzejewska R, Marusiak J, Kisiel-Sajewicz K, Jaskolska A (2007) Similar response of agonist and antagonist muscles after eccentric exercise revealed by electromyography and mechanomyography. J Electromyogr Kinesiol 17(5):568–577. doi:10.1016/j.jelekin.2006.05.002 CrossRefPubMed Jaskolski A, Andrzejewska R, Marusiak J, Kisiel-Sajewicz K, Jaskolska A (2007) Similar response of agonist and antagonist muscles after eccentric exercise revealed by electromyography and mechanomyography. J Electromyogr Kinesiol 17(5):568–577. doi:10.​1016/​j.​jelekin.​2006.​05.​002 CrossRefPubMed
go back to reference Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2+-ATPase in myotonic dystrophy type 1. Hum Mol Gen 14(15):2189–2200. doi:10.1093/hmg/ddi223 CrossRefPubMed Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2+-ATPase in myotonic dystrophy type 1. Hum Mol Gen 14(15):2189–2200. doi:10.​1093/​hmg/​ddi223 CrossRefPubMed
go back to reference Kornblum C, Lutterbey G, Bogdanow M, Kesper K, Schild H, Schroder R, Wattjes MP (2006) Distinct neuromuscular phenotypes in myotonic dystrophy types 1 and 2—a whole body highfield MRI study. J Neurol 253(6):753–761. doi:10.1007/s00415-006-0111-5 CrossRefPubMed Kornblum C, Lutterbey G, Bogdanow M, Kesper K, Schild H, Schroder R, Wattjes MP (2006) Distinct neuromuscular phenotypes in myotonic dystrophy types 1 and 2—a whole body highfield MRI study. J Neurol 253(6):753–761. doi:10.​1007/​s00415-006-0111-5 CrossRefPubMed
go back to reference Logigian EL, Moxley RTt, Blood CL, Barbieri CA, Martens WB, Wiegner AW, Thornton CA, Moxley RT 3rd (2004) Leukocyte CTG repeat length correlates with severity of myotonia in myotonic dystrophy type 1. Neurology 62(7):1081–1089CrossRef Logigian EL, Moxley RTt, Blood CL, Barbieri CA, Martens WB, Wiegner AW, Thornton CA, Moxley RT 3rd (2004) Leukocyte CTG repeat length correlates with severity of myotonia in myotonic dystrophy type 1. Neurology 62(7):1081–1089CrossRef
go back to reference Logigian EL, Blood CL, Dilek N, Martens WB, Moxley RTt, Wiegner AW, Thornton CA, Moxley RT 3rd (2005) Quantitative analysis of the “warm-up” phenomenon in myotonic dystrophy type 1. Muscle Nerve 32(1):35–42. doi:10.1002/mus.20339 CrossRefPubMed Logigian EL, Blood CL, Dilek N, Martens WB, Moxley RTt, Wiegner AW, Thornton CA, Moxley RT 3rd (2005) Quantitative analysis of the “warm-up” phenomenon in myotonic dystrophy type 1. Muscle Nerve 32(1):35–42. doi:10.​1002/​mus.​20339 CrossRefPubMed
go back to reference Logigian EL, Ciafaloni E, Quinn C, Dilek N, Pandya S, Moxley RT, Thornton CA (2007) Severity, type, and distribution of myotonic discharges are different in type 1 and type 2 myotonic dystrophy. Muscle Nerve 35(4):479–485. doi:10.1002/mus.20722 CrossRefPubMed Logigian EL, Ciafaloni E, Quinn C, Dilek N, Pandya S, Moxley RT, Thornton CA (2007) Severity, type, and distribution of myotonic discharges are different in type 1 and type 2 myotonic dystrophy. Muscle Nerve 35(4):479–485. doi:10.​1002/​mus.​20722 CrossRefPubMed
go back to reference Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, Moxley RT, Cannon SC, Thornton CA (2002) Expanded CUG repeats trigger aberrant splicing of CIC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10(1):35–44. doi:10.1016/S1097-2765(02)00563-4 CrossRefPubMed Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, Moxley RT, Cannon SC, Thornton CA (2002) Expanded CUG repeats trigger aberrant splicing of CIC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10(1):35–44. doi:10.​1016/​S1097-2765(02)00563-4 CrossRefPubMed
go back to reference Mano Y, Honda H, Takayanagi T (1985) Electrophysiological analysis of warming up phenomenon in myotonia. Jpn J Med 24(2):131–134CrossRef Mano Y, Honda H, Takayanagi T (1985) Electrophysiological analysis of warming up phenomenon in myotonia. Jpn J Med 24(2):131–134CrossRef
go back to reference Meola G (2013) Clinical aspects, molecular pathomechanisms and management of myotonic dystrophies. Acta Myol 32(3):154–165PubMedPubMedCentral Meola G (2013) Clinical aspects, molecular pathomechanisms and management of myotonic dystrophies. Acta Myol 32(3):154–165PubMedPubMedCentral
go back to reference Nakamori M, Sobczak K, Puwanant A, Welle S, Eichinger K, Pandya S, Dekdebrun J, Heatwole CR, McDermott MP, Chen T, Cline M, Tawil R, Osborne RJ, Wheeler TM, Swanson MS, Moxley RT 3rd, Thornton CA (2013) Splicing biomarkers of disease severity in myotonic dystrophy. Ann Neurol 74(6):862–872. doi:10.1002/ana.23992 CrossRefPubMedPubMedCentral Nakamori M, Sobczak K, Puwanant A, Welle S, Eichinger K, Pandya S, Dekdebrun J, Heatwole CR, McDermott MP, Chen T, Cline M, Tawil R, Osborne RJ, Wheeler TM, Swanson MS, Moxley RT 3rd, Thornton CA (2013) Splicing biomarkers of disease severity in myotonic dystrophy. Ann Neurol 74(6):862–872. doi:10.​1002/​ana.​23992 CrossRefPubMedPubMedCentral
go back to reference Orizio C, Esposito F, Paganotti I, Marino L, Rossi B, Veicsteinas A (1997a) Electrically-elicited surface mechanomyogram in myotonic dystrophy. It J Neurol Scis 18(4):185–190CrossRef Orizio C, Esposito F, Paganotti I, Marino L, Rossi B, Veicsteinas A (1997a) Electrically-elicited surface mechanomyogram in myotonic dystrophy. It J Neurol Scis 18(4):185–190CrossRef
go back to reference Orizio C, Esposito F, Sansone V, Parrinello G, Meola G, Veicsteinas A (1997b) Muscle surface mechanical and electrical activities in myotonic dystrophy. Electromyogr Clin Neurophysiol 37(4):231–239PubMed Orizio C, Esposito F, Sansone V, Parrinello G, Meola G, Veicsteinas A (1997b) Muscle surface mechanical and electrical activities in myotonic dystrophy. Electromyogr Clin Neurophysiol 37(4):231–239PubMed
go back to reference 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(3–4):326–336. doi:10.1007/s00421-003-0924-1 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(3–4):326–336. doi:10.​1007/​s00421-003-0924-1 CrossRefPubMed
go back to reference Smith CM, Housh TJ, Jenkins NDM, Hill EC, Cochrane KC, Miramonti AA, Schmidt RJ, Johnson GO (2016) Combining regression and mean comparisons to identify the time course of changes in neuromuscular responses during the process of fatigue. Physiol Meas 37(11):1993–2002. doi:10.1088/0967-3334/37/11/1993 CrossRefPubMed Smith CM, Housh TJ, Jenkins NDM, Hill EC, Cochrane KC, Miramonti AA, Schmidt RJ, Johnson GO (2016) Combining regression and mean comparisons to identify the time course of changes in neuromuscular responses during the process of fatigue. Physiol Meas 37(11):1993–2002. doi:10.​1088/​0967-3334/​37/​11/​1993 CrossRefPubMed
go back to reference Szmidt-Salkowska E, Gawel M, Lusakowska A, Nojszewska M, Lipowska M, Sulek A, Krysa W, Rajkiewicz M, Seroka A, Kaminska AM (2014) Does quantitative EMG differ myotonic dystrophy type 2 and type 1? J Electromyogr Kines 24(5):755–761. doi:10.1016/j.jelekin.2014.05.012 CrossRef Szmidt-Salkowska E, Gawel M, Lusakowska A, Nojszewska M, Lipowska M, Sulek A, Krysa W, Rajkiewicz M, Seroka A, Kaminska AM (2014) Does quantitative EMG differ myotonic dystrophy type 2 and type 1? J Electromyogr Kines 24(5):755–761. doi:10.​1016/​j.​jelekin.​2014.​05.​012 CrossRef
go back to reference Tang ZZ, Yarotskyy V, Wei L, Sobczak K, Nakamori M, Eichinger K, Moxley RT, Dirksen RT, Thornton CA (2012) Muscle weakness in myotonic dystrophy associated with misregulated splicing and altered gating of Ca(V)1.1 calcium channel. Hum Mol Gen 21(6):1312–1324. doi:10.1093/hmg/ddr568 CrossRefPubMed Tang ZZ, Yarotskyy V, Wei L, Sobczak K, Nakamori M, Eichinger K, Moxley RT, Dirksen RT, Thornton CA (2012) Muscle weakness in myotonic dystrophy associated with misregulated splicing and altered gating of Ca(V)1.1 calcium channel. Hum Mol Gen 21(6):1312–1324. doi:10.​1093/​hmg/​ddr568 CrossRefPubMed
go back to reference Taylor DC, Brooks DE, Ryan JB (1997) Viscoelastic characteristics of muscle: passive stretching versus muscular contractions. Med Sci Sports Exerc 29(12):1619–1624CrossRef Taylor DC, Brooks DE, Ryan JB (1997) Viscoelastic characteristics of muscle: passive stretching versus muscular contractions. Med Sci Sports Exerc 29(12):1619–1624CrossRef
go back to reference Tiffreau V, Detrembleur C, Van Den Bergh P, Renders A, Kinet V, Lejeune T (2012) Gait abnormalities in type 1 myotonic muscular dystrophy: 3D motion analysis, energy cost and surface EMG. Comput Methods Biomech Biomed Engin 15(Suppl 1):171–172. doi:10.1080/10255842.2012.713709 CrossRefPubMed Tiffreau V, Detrembleur C, Van Den Bergh P, Renders A, Kinet V, Lejeune T (2012) Gait abnormalities in type 1 myotonic muscular dystrophy: 3D motion analysis, energy cost and surface EMG. Comput Methods Biomech Biomed Engin 15(Suppl 1):171–172. doi:10.​1080/​10255842.​2012.​713709 CrossRefPubMed
go back to reference Viitasalo JT, Komi PV (1981) Interrelationships between electromyographic, mechanical, muscle structure and reflex time measurements in man. Acta Physiol Scand 111(1):97–103CrossRef Viitasalo JT, Komi PV (1981) Interrelationships between electromyographic, mechanical, muscle structure and reflex time measurements in man. Acta Physiol Scand 111(1):97–103CrossRef
go back to reference Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86(3):1086–1094CrossRef Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86(3):1086–1094CrossRef
Metadata
Title
Electromechanical delays during a fatiguing exercise and recovery in patients with myotonic dystrophy type 1
Authors
Fabio Esposito
Emiliano Cè
Susanna Rampichini
Elena Monti
Eloisa Limonta
Barbara Fossati
Giovanni Meola
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 3/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-017-3558-4

Other articles of this Issue 3/2017

European Journal of Applied Physiology 3/2017 Go to the issue