Neuromuscular electrical stimulation producing low evoked force elicits the repeated bout effect on muscle damage markers of the elbow flexors

Abstract

This study examined the repeated bout effect (RBE) on muscle damage markers following two bouts of neuromuscular electrical stimulation (NMES) in untrained individuals. Following familiarization, participants received 45 consecutive NMES to the biceps brachii at an intensity that produced low evoked force for the elbow flexors. Muscle damage markers (maximal voluntary isometric contraction [MVIC], elbow range of motion [ROM], muscle soreness via visual analogue scale [VAS] scores, pressure pain threshold [PPT], and muscle thickness) were measured before (PRE), after (POST), 1 day after (24 POST), and 2 days after (48 POST) NMES. Following 1 week of rest, procedures were replicated. Separate repeated measures two-way ANOVAs examined each measure. There were no interactions or bout main effects for MVIC or ROM. Time main effects indicated PRE MVIC was greater than POST (p ​= ​0.002) and 24-POST (p ​= ​0.024), and PRE ROM was greater than POST (p ​= ​0.036). There was no interaction for muscle thickness. Respective time and bout main effects indicated muscle thickness at PRE was less than POST (p ​= ​0.017), and second-bout muscle thickness (p ​= ​0.050) was less compared to the initial-bout. For PPT, there was an interaction (p ​= ​0.019). Initial-bout PRE PPT was less than POST (p ​= ​0.033). Initial-bout 48-POST PPT was less than second-bout 48-POST (p ​= ​0.037). There was a significant interaction for VAS (p ​= ​0.009). Initial-bout PRE VAS was less than POST (p ​= ​0.033) and 24-POST (p ​= ​0.015). Initial-bout POST and 24-POST VAS were greater than second-bout POST (p ​= ​0.023) and 24-POST (p ​= ​0.006), respectively. The results support RBE on muscle damage markers related to inflammation, but not MVIC and ROM.

Keywords

Muscle stimulation / Involuntary contraction / Muscle damage / Indirect muscle damage markers / Repeated bout effect

References

[[1]] R.D. Hyldahl, T.C. Chen, K. Nosaka. Mechanisms and mediators of the skeletal muscle repeated bout effect. Exerc Sport Sci Rev, 45 (1) ( 2017), pp. 24-33, DOI: 10.1249/JES.0000000000000095

[[2]] T.C. Chen, T.J. Yang, M.J. Huang, et al.. Damage and the repeated bout effect of arm, leg, and trunk muscles induced by eccentric resistance exercises. Scand J Med Sci Sports, 29 (5) ( 2019), pp. 725-735, DOI: 10.1111/sms.13388

[[3]] J. Škarabot, P. Ansdell, J. Temesi, G. Howatson, S. Goodall, R. Durbaba. Neurophysiological responses and adaptation following repeated bouts of maximal lengthening contractions in young and older adults. J Appl Physiol, 127 (5) ( 2019), pp. 1224-1237, DOI: 10.1152/japplphysiol.00494.2019

[[4]] S.S. Dias, M.G. Weber, S. Padoin, A.C. Andrello, E.I. Jussiani, S. de Paula Ramos. Circulating concentration of chemical elements during exercise-induced muscle damage and the repeated bout effect. Biol Trace Elem Res, 200 (3) ( 2022), pp. 1060-1070, DOI: 10.1007/s12011-021-02737-8

[[5]] A. Khassetarash, M. Baggaley, G. Vernillo, G.Y. Millet, W.B. Edwards.The repeated bout effect influences lower-extremity biomechanics during a 30-min downhill run. Eur J Sport Sci, 23 (4) ( 2023), pp. 510-519, DOI: 10.1080/17461391.2022.2048083

[[6]] T.C. Chen, H.L. Chen, Y.C. Liu, K. Nosaka. Eccentric exercise-induced muscle damage of pre-adolescent and adolescent boys in comparison to young men. Eur J Appl Physiol, 114 (6) ( 2014), pp. 1183-1195, DOI: 10.1007/s00421-014-2848-3

[[7]] G. Howatson, K. Van Someren, T. Hortobagyi. Repeated bout effect after maximal eccentric exercise. Int J Sports Med, 28 (7) ( 2007), pp. 557-563, DOI: 10.1055/s-2007-964866

[[8]] W.C. Tseng, K. Nosaka, K.W. Tseng, T.Y. Chou, T.C. Chen. Contralateral effects by unilateral eccentric versus concentric resistance training. Med Sci Sports Exerc, 52 (2) ( 2019), pp. 474-483, DOI: 10.1249/MSS.0000000000002155

[[9]] T.C. Chen, K. Nosaka, P. Sacco. Intensity of eccentric exercise, shift of optimum angle, and the magnitude of repeated-bout effect. J Appl Phys, 102 (3) ( 2007), pp. 992-999, DOI: 10.1152/japplphysiol.00425.2006

[[10]] S. Padoin, A.C. Zeffa, J.C.M. Corrêa, et al.. Phototherapy improves muscle recovery and does not impair repeated bout effect in plyometric exercise. J Strength Condit Res, 36 (12) ( 2022), pp. 3301-3310, DOI: 10.1519/JSC.0000000000003895

[[11]] T. Koeda, G. Mavropalias, K. Mizumura, K. Katanosaka, K. Nosaka. Changes in nerve growth factor in vastus lateralis muscle after the first versus second bout of one leg eccentric cycling. Scand J Med Sci Sports, 34 (1) ( 2024), Article e14497, DOI: 10.1111/sms.14497

[[12]] A.P. Lavender, K. Nosaka. Responses of old men to repeated bouts of eccentric exercise of the elbow flexors in comparison with young men. Eur J Appl Physiol, 97 (5) ( 2006), pp. 619-626, DOI: 10.1007/s00421-006-0224-7

[[13]] M.J. Falvo, B.K. Schilling, R.J. Bloomer, W.A. Smith.Repeated bout effect is absent in resistance trained men: an electromyographic analysis. J Electromyogr Kinesiol, 19 (6) ( 2009), pp. e529-e535, DOI: 10.1016/j. jelekin.2008.10.010

[[14]] E. Ochi, H. Ueda, Y. Tsuchiya, K. Nakazato. Eccentric exercise causes delayed sensory nerve conduction velocity but no repeated bout effect in the flexor pollicis brevis muscles. Eur J Appl Physiol, 121 (11) ( 2021), pp. 3069-3081, DOI: 10.1007/s00421-021-04773-7

[[15]] D.A. Connolly, B.V. Reed, M.P. McHugh. The repeated bout effect: does evidence for a crossover effect exist?. J Sports Sci Med, 1 (3) ( 2002), pp. 80-86

[[16]] N.A. Maffiuletti, M.A. Minetto, D. Farina, R. Bottinelli. Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol, 111 (10) ( 2011), pp. 2391-2397, DOI: 10.1007/s00421-011-2133-7

[[17]] M.L. Dirks, B.T. Wall, T. Snijders, C.L. Ottenbros, L.B. Verdijk, L.J. van Loon. Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol, 210 (3) ( 2014), pp. 628-641, DOI: 10.1111/apha.12200

[[18]] N. Babault, G. Cometti, M. Bernardin, M. Pousson, J.C. Chatard. Effects of electromyostimulation training on muscle strength and power of elite rugby players. J Strength Condit Res, 21 (2) ( 2007), pp. 431-437, DOI: 10.1519/R-19365.1

[[19]] A.L. Mackey, J. Bojsen-Moller, K. Qvortrup, et al.. Evidence of skeletal muscle damage following electrically stimulated isometric muscle contractions in humans. J Appl Phys, 105 (5) ( 2008), pp. 1620-1627, DOI: 10.1152/japplphysiol.90952.2008

[[20]] M. Jubeau, M. Muthalib, G.Y. Millet, N.A. Maffiuletti, K. Nosaka. Comparison in muscle damage between maximal voluntary and electrically evoked isometric contractions of the elbow flexors. Eur J Appl Physiol, 112 (2) ( 2012), pp. 429-438, DOI: 10.1007/s00421-011-1991-3

[[21]] N.A. Maffiuletti. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol, 110 (2) ( 2010), pp. 223-234, DOI: 10.1007/s00421-010-1502-y

[[22]] M.P. McHugh, S. Pasiakos. The role of exercising muscle length in the protective adaptation to a single bout of eccentric exercise. Eur J Appl Physiol, 93 (3) ( 2004), pp. 286-293, DOI: 10.1007/s00421-004-1196-0

[[23]] A. Aldayel, M. Jubeau, M.R. McGuigan, K. Nosaka. Less indication of muscle damage in the second than initial electrical muscle stimulation bout consisting of isometric contractions of the knee extensors. Eur J Appl Physiol, 108 (4) ( 2010), pp. 709-717, DOI: 10.1007/s00421-009-1278-0

[[24]] K. Nosaka, M. Newton, P. Sacco. Responses of human elbow flexor muscles to electrically stimulated forced lengthening exercise. Acta Physiol Scand, 174 (2) ( 2002), pp. 137-145, DOI: 10.1046/j.1365-201X.2002.00936.x

[[25]] C.D. Black, K.K. McCully. Muscle injury after repeated bouts of voluntary and electrically stimulated exercise. Med Sci Sports Exerc, 40 (9) ( 2008), pp. 1605-1615, DOI: 10.1249/MSS.0b013e3181788dbe

[[26]] N.A. Maffiuletti, J. Gondin, N. Place, J. Stevens-Lapsley, I. Vivodtzev, M.A. Minetto. Clinical use of neuromuscular electrical stimulation for neuromuscular rehabilitation: what are we overlooking?. Arch Phys Med Rehabil, 99 (4) ( 2018), pp. 806-812, DOI: 10.1016/j.apmr.2017.10.028

[[27]] G.J. Almeida, S.S. Khoja, S.R. Piva. Dose-response relationship between neuromuscular electrical stimulation and muscle function in people with rheumatoid arthritis. Phys Ther, 99 (9) ( 2019), pp. 1167-1176, DOI: 10.1093/ptj/pzz079

[[28]] A. Fouré, J. Gondin. Skeletal muscle damage produced by electrically evoked muscle contractions. Exerc Sport Sci Rev, 49 (1) ( 2021), pp. 59-65, DOI: 10.1249/JES.0000000000000239

[[29]] A. Sartorio, M. Jubeau, F. Agosti, et al.. GH responses to two consecutive bouts of neuromuscular electrical stimulation in healthy adults. Eur J Endocrinol, 158 (3) ( 2008), pp. 311-316, DOI: 10.1530/EJE-07-0775

[[30]] S. Jeon, M. Kang, X. Ye. Contralateral protective effect against repeated bout of damaging exercise: a meta-analysis. Res Sports Med, 31 (2) ( 2023), pp. 137-156, DOI: 10.1080/15438627.2021.1954512

[[31]] X. Ye, R.J. Benton, W.M. Miller, S. Jeon, J.S. Song. Downhill running impairs peripheral but not central neuromuscular indices in elbow flexor muscles. Sports Med Health Sci, 3 (2) ( 2021), pp. 101-109, DOI: 10.1016/j.smhs.2021.03.001

[[32]] B.R. Bowman, L.L. Baker. Effects of waveform parameters on comfort during transcutaneous neuromuscular electrical stimulation. Ann Biomed Eng, 13 (1) ( 1985), pp. 59-74, DOI: 10.1007/BF02371250

[[33]] M. Jubeau, A. Sartorio, P.G. Marinone, et al.. Comparison between voluntary and stimulated contractions of the quadriceps femoris for growth hormone response and muscle damage. J Appl Physiol, 104 (1) ( 2008), pp. 75-81, DOI: 10.1152/japplphysiol.00335.2007

[[34]] J. Laurin, E. Dousset, R. Carrivale, L. Grélot, P. Decherchi. Recovery pattern of motor reflex after a single bout of neuromuscular electrical stimulation session. Scand J Med Sci Sports, 22 (4) ( 2012), pp. 534-544, DOI: 10.1111/j.1600-0838.2010.01279.x

[[35]] K. Nosaka, K. Sakamoto. Effect of elbow joint angle on the magnitude of muscle damage to the elbow flexors. Med Sci Sports Exerc, 33 (1) ( 2001), pp. 22-29, DOI: 10.1097/00005768-200101000-00005

[[36]] W.Y. Lau, A.J. Blazevich, M.J. Newton, S.S. Wu, K. Nosaka. Assessment of muscle pain induced by elbow-flexor eccentric exercise. J Athl Train, 50 (11) ( 2015), pp. 1140-1148, DOI: 10.4085/1062-6050-50.11.05

[[37]] T.C. Chen, H.L. Chen, M.J. Lin, H.I. Yu, K. Nosaka. Contralateral repeated bout effect of eccentric exercise of the elbow flexors. Med Sci Sports Exerc, 48 (10) ( 2016), pp. 2030-2039, DOI: 10.1249/mss.0000000000000991

[[38]] E. Chalchat, J. Siracusa, C. Bourrilhon, K. Charlot, V. Martin, S. Garcia-Vicencio. Muscle shear elastic modulus provides an indication of the protection conferred by the repeated bout effect. Front Physiol, 13 ( 2022), Article 877485, DOI: 10.3389/fphys.2022.877485

[[39]] S. Jeon, X. Ye, W.M. Miller, J.S. Song. Effect of repeated eccentric exercise on muscle damage markers and motor unit control strategies in arm and hand muscle. Sports Med Health Sci, 4 (1) ( 2022), pp. 44-53, DOI: 10.1016/j.smhs.2021.12.002

[[40]] T.C. Chen, S.H. Wu, H.L. Chen, et al.. Effects of unilateral eccentric versus concentric training of nonimmobilized arm during immobilization. Med Sci Sports Exerc, 55 (7) ( 2023), pp. 1195-1207, DOI: 10.1249/MSS.0000000000003140

[[41]] S.F. van Rijn, E.L. Zwerus, K.L. Koenraadt, W.C. Jacobs, M.P. van den Bekerom, D. Eygendaal. The reliability and validity of goniometric elbow measurements in adults: a systematic review of the literature. Shoulder Elbow, 10 (4) ( 2018), pp. 274-284, DOI: 10.1177/1758573218774326

[[42]] A. Fouré, K. Nosaka, J. Wegrzyk, et al.. Time course of central and peripheral alterations after isometric neuromuscular electrical stimulation-induced muscle damage. PLoS One, 9 (9) ( 2014), Article e107298, DOI: 10.1371/journal.pone.0107298

[[43]] E. Jówko, M. Płaszewski, M. Cieśliński, T. Sacewicz, I. Cieśliński, M. Jarocka. The effect of low level laser irradiation on oxidative stress, muscle damage and function following neuromuscular electrical stimulation. A double blind, randomised, crossover trial. BMC Sports Sci Med Rehabil, 11 ( 2019), pp. 1-14, DOI: 10.1186/s13102-019-0147-3

[[44]] M. Jubeau, J. Gondin, A. Martin, A. Sartorio, N.A. Maffiuletti. Random motor unit activation by electrostimulation. Int J Sports Med, 28 (11) ( 2007), pp. 901-904, DOI: 10.1055/s-2007-965075

[[45]] T.S. Barss, E.N. Ainsley, F.C. Claveria-Gonzalez, et al.. Utilizing physiological principles of motor unit recruitment to reduce fatigability of electrically-evoked contractions: a narrative review. Arch Phys Med Rehabil, 99 (4) ( 2018), pp. 779-791, DOI: 10.1016/j.apmr.2017.08.478

[[46]] M. Vanderthommen, R. Chamayou, C. Demoulin, J.M. Crielaard, J.L. Croisier. Protection against muscle damage induced by electrical stimulation: efficiency of a preconditioning programme. Clin Physiol Funct Imag, 35 (4) ( 2015), pp. 267-274, DOI: 10.1111/cpf.12160

[[47]] R. Zory, D. Boërio, M. Jubeau, N.A. Maffiuletti. Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med, 26 (10) ( 2005), pp. 847-853, DOI: 10.1055/s-2005-837459

[[48]] S. Racinais, O. Girard, J.P. Micallef, S. Perrey. Failed excitability of spinal motoneurons induced by prolonged running exercise. J Neurophysiol, 97 (1) ( 2007), pp. 596-603, DOI: 10.1152/jn.00903.2006

[[49]] E. Chalchat, E. Piponnier, B. Bontemps, et al.. Characteristics of motor unit recruitment in boys and men at maximal and submaximal force levels. Exp Brain Res, 237 (5) ( 2019), pp. 1289-1302, DOI: 10.1007/s00221-019-05508-z

[[50]] M. Trevino, A. Sterczala, J. Miller, et al.. Sex-related differences in muscle size explained by amplitudes of higher-threshold motor unit action potentials and muscle fibre typing. Acta Physiol, 225 (4) ( 2019), Article e13151, DOI: 10.1111/apha.13151

[[51]] A.A. Olmos, A.J. Sterczala, M.E. Parra, et al.. Sex-related differences in motor unit behavior are influenced by myosin heavy chain during high but not moderate intensity contractions. Acta Physiol, 239 (1) ( 2023), Article e14024, DOI: 10.1111/apha.14024

[[52]] A.J. Meneghel, A.H. Crisp, R. Verlengia, C.R. Lopes. Review the repeated bout effect in resistance. Int J Sports Sci, 3 (4) ( 2013), pp. 107-114, DOI: 10.5923/j.sports.20130304.03

[[53]] P.M. Clarkson, K. Nosaka, B. Braun. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc, 24 (5) ( 1992), pp. 512-520

[[54]] T.W. Buford, M.B. Cooke, B.D. Shelmadine, G.M. Hudson, L. Redd, D.S. Willoughby. Effects of eccentric treadmill exercise on inflammatory gene expression in human skeletal muscle. Appl Physiol Nutr Metabol, 34 (4) ( 2009), pp. 745-753, DOI: 10.1139/H09-067

[[55]] K. Nosaka, P.M. Clarkson. Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exerc, 28 (8) ( 1996), pp. 953-961, DOI: 10.1097/00005768-199608000-00003

[[56]] T.C. Chen, M.J. Lin, J.H. Lai, H.L. Chen, H.I. Yu, K. Nosaka. Low-intensity elbow flexion eccentric contractions attenuate maximal eccentric exercise-induced muscle damage of the contralateral arm. J Sci Med Sport, 21 (10) ( 2018), pp. 1068-1072, DOI: 10.1016/j.jsams.2017.12.012

[[57]] E.L. Nussbaum, P. Houghton, J. Anthony, S. Rennie, B.L. Shay, A.M. Hoens. Neuromuscular electrical stimulation for treatment of muscle impairment: critical review and recommendations for clinical practice. Physiother Can, 69 (5) ( 2017), pp. 1-76, DOI: 10.3138/ptc.2015-88

[[58]] N.R. Glaviano, S. Saliba. Can the use of neuromuscular electrical stimulation be improved to optimize quadriceps strengthening?. Sport Health, 8 (1) ( 2016), pp. 79-85, DOI: 10.1177/1941738115618174

[[59]] B.J. Broderick, C. Kennedy, P.P. Breen, S.R. Kearns, G. Ólaighin. Patient tolerance of neuromuscular electrical stimulation (NMES) in the presence of orthopaedic implants. Med Eng Phys, 33 (1) ( 2011), pp. 56-61, DOI: 10.1016/j.medengphy.2010.09.003

[[60]] G. Mavropalias, T. Koeda, O.R. Barley, et al.. Comparison between high-and low-intensity eccentric cycling of equal mechanical work for muscle damage and the repeated bout effect. Eur J Appl Physiol, 120 (5) ( 2020), pp. 1015-1025, DOI: 10.1007/s00421-020-04341-5

The authors would like to thank all the participants who took time out of their schedules to help with these projects.