Sex- and Mode-specific Responses to Eccentric Muscle Fatigue

Abstract

The primary purpose of the present investigation was to examine sex-related differences as a result of fatiguing eccentric muscle actions on torque, muscle blood flow, electromyography, and mechanomyography. Eighteen men and 18 women performed peak torque trials prior to (pretest), immediately after (posttest), and 5-min after (recovery) completing 50 submaximal (60% of eccentric peak torque), eccentric, isokinetic (180°·s ⁻¹) muscle actions of the elbow flexors. Electromyographic and mechanomyographic responses were simultaneously recorded from the biceps brachii muscle, and muscle blood flow was measured at pretest, posttest and recovery. There were sex- and mode-specific responses for torque, but there were no sex-specific muscle blood flow or neuromuscular responses. From pretest to posttest, torque decreased (80.0–88.2% of pretest) for both the men and women. At recovery concentric peak torque recovered to a greater extent in women (95.0% of pretest) than men (88.0% of pretest), while eccentric peak torque recovered to a greater extent in men (88.9% of pretest) than women (86.9% of pretest). The sex-specific torque responses were not associated with different motor control strategies or differences in the occlusion of muscle blood flow between the men and women. For both men and women, eccentric fatiguing exercise is manifested similarly during isometric muscle actions, but not during eccentric and concentric muscle actions.

Key words

blood flow - motor control - isokinetic - muscle fatigue - gender - EMG - MMG

• References

• 1 Arendt-Nielsen L, Mills KR, Forster A. Changes in muscle fiber conduction velocity, mean power frequency, and mean EMG voltage during prolonged submaximal contractions. Muscle Nerve 1989; 12: 493-497
• 2 Babault N, Desbrosses K, Fabre M-S, Michaut A, Pousson M. Neuromuscular fatigue development during maximal concentric and isometric knee extensions. J Appl Physiol 2006; 100: 780-785
• 3 Barbero M, Merletti R, Rainoldi A. Atlas of Muscle Innervation Zones Understanding Surface Electromyography and its Applications. New York, NY: Springer; 2012
• 4 Beck TW, Housh TJ, Cramer JT, Weir JP, Johnson GO, Coburn JW, Malek MH, Mielke M. Mechanomyographic amplitude and frequency responses during dynamic muscle actions: A comprehensive review. Biomed Engin 2005; 4: 67
• 5 Brown LE, Whitehurst M, Gilbert R, Buchalter DN. The effect of velocity and gender on load range during knee extension and flexion exercise on an isokinetic device. J Orthop Sports Phys Ther 1995; 21: 107-112
• 6 Brughelli M, Cronin J. Altering the length-tension relationship with eccentric exercise: Implications for performance and injury. Sports Med 2007; 37: 807-826
• 7 Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: A report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39: 257-265
• 8 Gassner M, Killu K, Bauman Z, Coba V, Rosso K, Blyden D. Feasibility of common carotid artery point of care ultrasound in cardiac output measurements compared to invasive methods. J Ultrasound 2015; 18: 127-133
• 9 Gil AL, Neto GR, Sousa MS, Dias I, Vianna J, Nunes RA, Novaes JS. Effect of strength training with blood flow restriction on muscle power and submaximal strength in eumenorrheic women. Clin Physiol Funct Imaging 2017; 37: 221-228
• 10 Guilhem G, Cornu C, Guevel A. Neuromuscular and muscle-tendon system adaptations to isotonic and isokinetic eccentric exercise. Ann Phys Rehabil Med 2010; 53: 319-341
• 11 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 Update. Int J Sports Med 2017; 38: 1126-1131
• 12 Hashimoto M, Akishita M, Eto M, Ishikawa M, Kozaki K, Toba K, Sagara Y, Taketani Y, Orimo H, Ouchi Y. Modulation of endothelium-dependent flow-mediated dilatation of the brachial artery by sex and menstrual cycle. Circulation 1995; 92: 3431-3435
• 13 Herzog W. Mechanisms of enhanced force production in lengthening (eccentric) muscle contractions. J Appl Physiol 2014; 116: 1407-1417
• 14 Hicks AL, Kent-Braun J, Ditor DS. Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev 2001; 29: 109-112
• 15 Hill E, Housh T, Smith C, Cochrane K, Jenkins N, Schmidt R, Johnson G. Muscle- and mode-specific responses of the forearm flexors in women as a result of fatiguing, concentric muscle actions. Int J Phys Educ Sports Health 2016; 3: 431-438
• 16 Hill E, Housh T, Smith C, Schmidt R, Johnson G. Muscle- and mode-specific responses of the forearm flexors to fatiguing, concentric muscle actions. Sports (Basel) 2016; 4: 47
• 17 Hill EC, Housh TJ, Keller JL, Smith CM, Schmidt RJ, Johnson GO. Gender- and muscle- specific responses during fatiguing exercise. J Strength Cond Res 2018; 32: 1471-1478
• 18 Hill EC, Housh TJ, Smith CM, Cochrane KC, Jenkins NDM, Cramer JT, Schmidt RJ, Johnson GO. Effect of sex on torque, recovery, EMG, and MMG responses to fatigue. J Musculoskelet Neuronal Interact 2016; 16: 310-317
• 19 Hill EC, Housh TJ, Smith CM, Keller JL, Schmidt RJ, Johnson GO. The contributions of arterial cross-sectional area and time-averaged flow velocity to arterial blood flow. J Med Ultrasound 2018, Epub doi:10.4103/JMU.JMU_20_18
• 20 Hunter SK. Sex differences in human fatigability: Mechanisms and insight to physiological responses. Acta Physiol (Oxf) 2014; 210: 768-789
• 21 Hunter SK. Sex differences in fatigability of dynamic contractions. Exp Physiol 2016; 101: 250-255
• 22 Hunter SK, Butler JE, Todd G, Gandevia SC, Taylor JL. Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol 2006; 101: 1036-1044
• 23 Hunter SK, Critchlow A, Shin IS, Enoka RM. Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J Appl Physiol 2004; 96: 195-202
• 24 Hunter SK, Enoka RM. Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol 2001; 91: 2686-2694
• 25 Jackson AS, Pollock ML. Practical assessment of body composition. Phys Sportsmed 1985; 13: 76-90
• 26 Kang T, Seo Y, Park J, Dong E, Seo B, Han D. The effects of elbow joint angle change on the elbow flexor muscle activation in pulley with weight exercise. J Phys Ther Sci 2013; 25: 1133-1136
• 27 Kent-Braun JA, Ng AV, Doyle JW, Towse TF. Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 2002; 93: 1813-1823
• 28 Krejza J, Mariak Z, Huba M, Wolczynski S, Lewko J. Effect of endogenous estrogen on blood flow through carotid arteries. Stroke 2001; 32: 30-36
• 29 Lee A, Baxter J, Eischer C, Gage M, Hunter S, Yoon T. Sex differences in neuromuscular function after repeated eccentric contractions of the knee extensor muscles. Eur J Appl Physiol 2017; 117: 1119-1130
• 30 Levenson J, Pessana F, Gariepy J, Armentano R, Simon A. Gender differences in wall shear-mediated brachial artery vasoconstriction and vasodilation. J Am Coll Cardiol 2001; 38: 1668-1674
• 31 Mattacola CG, Perrin DH, Gansneder BM, Allen JD, Mickey CA. A comparison of visual analog and graphic rating scales for assessing pain following delayed onset muscle soreness. J Sport Rehab 1997; 6: 38-46
• 32 Maughan RJ, Harmon M, Leiper JB, Sale D, Delman A. Endurance capacity of untrained males and females in isometric and dynamic muscular contractions. Eur J Appl Physiol Occup Physiol 1986; 55: 395-400
• 33 McHugh MP, Tyler TF, Greenberg SC, Gleim GW. Differences in activation patterns between eccentric and concentric quadriceps contractions. J Sports Sci 2002; 20: 83-91
• 34 Nardone A, Romano C, Schieppati M. Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J Physiol 1989; 409: 451-471
• 35 Nichols AW, Hetzler RK, Villanueva RJ, Stickley CD, Kimura IF. Effects of combination oral contraceptives on strength development in women athletes. J Strength Cond Res 2008; 22: 1625-1632
• 36 Orizio C, Gobbo M, Diemont B, Esposito F, Veicsteinas A. 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 2003; 90: 326-336
• 37 Osada T, Murase N, Kime R, Katsumura T, Rådegran G. Blood flow dynamics in the limb conduit artery during dynamic knee extensor exercise assessed by continuous Doppler ultrasound measurements. J Phys Fit Sports Med 2014; 3: 409-421
• 38 Osada T, Radegran G. Alterations in the blood velocity profile influence the blood flow response during muscle contractions and relaxations. J Physiol Sci 2006; 56: 195-203
• 39 Parker BA, Smithmyer SL, Pelberg JA, Mishkin AD, Herr MD, Proctor DN. Sex differences in leg vasodilation during graded knee extensor exercise in young adults. J Appl Physiol 2007; 103: 1583-1591
• 40 Power GA, Dalton BH, Rice CL, Vandervoort AA. Delayed recovery of velocity- dependent power loss following eccentric actions of the ankle dorsiflexors. J Appl Physiol 2010; 109: 669-676
• 41 Power GA, Dalton BH, Rice CL, Vandervoort AA. Peak power is reduced following lengthening contractions despite a maintenance of shortening velocity. Appl Physiol Nutr Metab 2013; 38: 1196-1205
• 42 Prasartwuth O, Allen TJ, Butler JE, Gandevia SC, Taylor JL. Length-dependent changes in voluntary activation, maximum voluntary torque and twitch responses after eccentric damage in humans. J Physiol 2006; 571: 243-252
• 43 Russ DW, Kent-Braun JA. Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol 2003; 94: 2414-2422
• 44 Sakamaki M, Yasuda T, Abe T. Comparison of low-intensity blood flow-restricted training-induced muscular hypertrophy in eumenorrheic women in the follicular phase and luteal phase and age-matched men. Clin Physiol Funct Imaging 2012; 32: 185-191
• 45 Sarwar R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatiguability during the human menstrual cycle. J Physiol 1996; 493: 267-272
• 46 Sayers SP, Clarkson PM. Force recovery after eccentric exercise in males and females. Eur J Appl Physiol 2001; 84: 122-126
• 47 Senefeld J, Pereira HM, Elliott N, Yoon T, Hunter SK. Sex differences in mechanisms of recovery after isometric and dynamic fatiguing tasks. Med Sci Sports Exerc 2018; 50: 1070-1083
• 48 Senefeld J, Yoon T, Bement MH, Hunter SK. Fatigue and recovery from dynamic contractions in men and women differ for arm and leg muscles. Muscle Nerve 2013; 48: 436-439
• 49 Sewright KA, Hubal MJ, Kearns A, Holbrook MT, Clarkson PM. Sex differences in response to maximal eccentric exercise. Med Sci Sports Exerc 2008; 40: 242-251
• 50 Solomonow M, Baratta R, Zhou BH, D’Ambrosia R. Electromyogram coactivation patterns of the elbow antagonist muscles during slow isokinetic movement. Exp Neurol 1988; 100: 470-477
• 51 Sung E, Han A, Hinrichs T, Vorgerd M, Manchado C, Platen P. Effects of follicular versus luteal phase-based strength training in young women. SpringerPlus 2014; 3: 668
• 52 Wakeling JM, Uehli K, Rozitis AI. Muscle fibre recruitment can respond to the mechanics of the muscle contraction. J R Soc Interface 2006; 3: 533-544
• 53 Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res 2005; 19: 231-240
• 54 Wikstrom-Frisen L, Boraxbekk CJ, Henriksson-Larsen K. Effects on power, strength and lean body mass of menstrual/oral contraceptive cycle based resistance training. J Sport Med Phys Fitness 2017; 57: 43-52
• 55 Williams MR, Westerman RA, Kingwell BA, Paige J, Blombery PA, Sudhir K, Komesaroff PA. Variations in endothelial function and arterial compliance during the menstrual cycle. J Clin Endocrin Metab 2001; 86: 5389-5395
• 56 Yoon T, Doyel R, Widule C, Hunter SK. Sex differences with aging in the fatigability of dynamic contractions. Exp Gerontol 2015; 70: 1-10