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01-01-2016 | Original Article

Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling

Authors: Felipe Damas, Stuart M. Phillips, Manoel E. Lixandrão, Felipe C. Vechin, Cleiton A. Libardi, Hamilton Roschel, Valmor Tricoli, Carlos Ugrinowitsch

Published in: European Journal of Applied Physiology | Issue 1/2016

Abstract

Purpose

It has been proposed that skeletal muscle shows signs of resistance training (RT)-induced muscle hypertrophy much earlier (i.e., ~3–4 weeks of RT) than previously thought. We determined if early increases in whole muscle cross-sectional area (CSA) during a period of RT were concomitant with edematous muscle swelling and thus not completely attributable to hypertrophy.

Methods

We analyzed vastus lateralis muscle ultrasound CSA images and their respective echo intensities (CSA-US_echo) at the beginning (T1), in the 3rd week of RT (T2) and at the end (T3) of a 10-week RT period in ten untrained young men. Functional parameters [training volume (TV = load × reps × sets) and maximal voluntary contraction (MVC)] and muscle damage markers (myoglobin and interleukin-6) were also assessed.

Result

Muscle CSA increased significantly at T2 (~2.7 %) and T3 (~10.4 %) versus T1. Similarly, CSA-US_echo increased at T2 (~17.2 %) and T3 (~13.7 %). However, when CSA-US_echo was normalized to the increase in muscle CSA, only T2 showed a significantly higher US_echo versus T1. Additionally, TV increased at T2 and T3 versus T1, but MVC increased only at T3. Myoglobin and Interleukin-6 were elevated at T2 versus T1, and myoglobin was also higher at T2 versus T3.

Conclusion

We propose that early RT-induced increases in muscle CSA in untrained young individuals are not purely hypertrophy, since there is concomitant edema-induced muscle swelling, probably due to muscle damage, which may account for a large proportion of the increase. Therefore, muscle CSA increases (particularly early in an RT program) should not be labeled as hypertrophy without some concomitant measure of muscle edema/damage.

Berg HE, Tedner B, Tesch PA (1993) Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol Scand 148(4):379–385. doi:10.1111/j.1748-1716.1993.tb09573.x PubMedCrossRef

Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, Holwerda AM, Parise G, Rennie MJ, Baker SK, Phillips SM (2010) Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS One 5(8):e12033. doi:10.1371/journal.pone.0012033 PubMedPubMedCentralCrossRef

Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ (2012) Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr 96(6):1454–1464. doi:10.3945/ajcn.112.037556 PubMedCrossRef

Chen TC, Nosaka K (2006) Responses of elbow flexors to two strenuous eccentric exercise bouts separated by three days. J Strength Cond Res 20(1):108–116PubMed

Chen TC, Chen HL, Lin MJ, Wu CJ, Nosaka K (2009) Muscle damage responses of the elbow flexors to four maximal eccentric exercise bouts performed every 4 weeks. Eur J Appl Physiol 106(2):267–275PubMedCrossRef

Chen HL, Nosaka K, Pearce AJ, Chen TC (2012) Two maximal isometric contractions attenuate the magnitude of eccentric exercise-induced muscle damage. Appl Physiol Nutr Metab 37(4):680–689. doi:10.1139/h2012-035 PubMedCrossRef

Chen TC, Chen HL, Lin MJ, Chen CH, Pearce AJ, Nosaka K (2013) Effect of two maximal isometric contractions on eccentric exercise-induced muscle damage of the elbow flexors. Eur J Appl Physiol 113(6):1545–1554. doi:10.1007/s00421-012-2581-8 PubMedCrossRef

Conceição MS, Libardi CA, Nogueira FR, Bonganha V, Gaspari AF, Chacon-Mikahil MP, Cavaglieri CR, Madruga VA (2012) Effects of eccentric exercise on systemic concentrations of pro- and anti-inflammatory cytokines and prostaglandin (E2): comparison between young and postmenopausal women. Eur J Appl Physiol 112(9):3205–3213. doi:10.1007/s00421-011-2292-6 PubMedCrossRef

Damas F, Phillips S, Vechin FC, Ugrinowitsch C (2015) A review of resistance training-induced changes in skeletal muscle protein synthesis and their contribution to hypertrophy. Sports Med 45(6):801–807. doi:10.1007/s40279-015-0320-0 PubMedCrossRef

DeFreitas JM, Beck TW, Stock MS, Dillon MA, Kasishke PR 2nd (2011) An examination of the time course of training-induced skeletal muscle hypertrophy. Eur J Appl Physiol 111(11):2785–2790. doi:10.1007/s00421-011-1905-4 PubMedCrossRef

Fleckenstein JL, Canby RC, Parkey RW, Peshock RM (1988) Acute effects of exercise on MR imaging of skeletal muscle in normal volunteers. AJR Am J Roentgenol 151(2):231–237. doi:10.2214/ajr.151.2.231 PubMedCrossRef

Fujikake T, Hart R, Nosaka K (2009) Changes in B-mode ultrasound echo intensity following injection of bupivacaine hydrochloride to rat hind limb muscles in relation to histologic changes. Ultrasound Med Biol 35(4):687–696. doi:10.1016/j.ultrasmedbio.2008.10.008 PubMedCrossRef

Gonzalez-Izal M, Lusa Cadore E, Izquierdo M (2014) Muscle conduction velocity, surface electromyography variables, and echo intensity during concentric and eccentric fatigue. Muscle Nerve 49(3):389–397PubMedCrossRef

Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV, Phillips SM (2007) Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Am J Clin Nutr 86(2):373–381PubMed

Kamen G, Knight CA (2004) Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59(12):1334–1338PubMedCrossRef

Krentz JR, Farthing JP (2010) Neural and morphological changes in response to a 20-day intense eccentric training protocol. Eur J Appl Physiol 110(2):333–340. doi:10.1007/s00421-010-1513-8 PubMedCrossRef

Lixandrao ME, Ugrinowitsch C, Bottaro M, Chacon-Mikahil MP, Cavaglieri CR, Min LL, de Souza EO, Laurentino GC, Libardi CA (2014) Vastus Lateralis muscle cross-sectional area ultrasonography validity for image fitting in humans. J Strength Cond Res 28(11):3293–3297. doi:10.1519/JSC.0000000000000532 PubMedCrossRef

May DA, Disler DG, Jones EA, Balkissoon AA, Manaster BJ (2000) Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls, and pitfalls. Radiographics 20 Spec No:S295-315. doi:10.1148/radiographics.20.suppl_1.g00oc18s295

Mitchell CJ, Churchward-Venne TA, West DW, Burd NA, Breen L, Baker SK, Phillips SM (2012) Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J Appl Physiol 113(1):71–77. doi:10.1152/japplphysiol.00307.2012 PubMedPubMedCentralCrossRef

Moritani T, deVries HA (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58(3):115–130PubMed

Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc 82(4):591–605. doi:10.1111/j.1469-185X.2007.00027.x PubMedCrossRef

Newham DJ, Jones DA, Clarkson PM (1987) Repeated high-force eccentric exercise: effects on muscle pain and damage. J Appl Physiol 63(4):1381–1386PubMed

Nosaka K, Clarkson PM (1996) Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exerc 28(8):953–961PubMedCrossRef

Nosaka K, Sakamoto K (2001) Effect of elbow joint angle on the magnitude of muscle damage to the elbow flexors. Med Sci Sports Exerc 33(1):22–29PubMedCrossRef

Nosaka K, Newton MJ, Sacco P (2005) Attenuation of protective effect against eccentric exercise-induced muscle damage. Can J Appl Physiol 30(5):529–542PubMedCrossRef

Phillips SM (2000) Short-term training: when do repeated bouts of resistance exercise become training? Can J Appl Physiol 25(3):185–193PubMedCrossRef

Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273(1 Pt 1):E99–107PubMed

Pillen S, van Alfen N (2011) Skeletal muscle ultrasound. Neurol Res 33(10):1016–1024. doi:10.1179/1743132811Y.0000000010 PubMedCrossRef

Rosenberg JG, Ryan ED, Sobolewski EJ, Scharville MJ, Thompson BJ, King GE (2014) Reliability of panoramic ultrasound imaging to simultaneously examine muscle size and quality of the medial gastrocnemius. Muscle Nerve 49(5):736–740. doi:10.1002/mus.24061 PubMedCrossRef

Sale DG, Martin JE, Moroz DE (1992) Hypertrophy without increased isometric strength after weight training. Eur J Appl Physiol Occup Physiol 64(1):51–55PubMedCrossRef

Seynnes OR, de Boer M, Narici MV (2007) Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 102(1):368–373. doi:10.1152/japplphysiol.00789.2006 PubMedCrossRef

Smith LL, Anwar A, Fragen M, Rananto C, Johnson R, Holbert D (2000) Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol 82(1–2):61–67. doi:10.1007/s004210050652 PubMedCrossRef

Sorichter S, Puschendorf B, Mair J (1999) Skeletal muscle injury induced by eccentric muscle action: muscle proteins as markers of muscle fiber injury. Exerc Immunol Rev 5:5–21PubMed

Tang JE, Perco JG, Moore DR, Wilkinson SB, Phillips SM (2008) Resistance training alters the response of fed state mixed muscle protein synthesis in young men. Am J Physiol Regul Integr Comp Physiol 294(1):R172–R178. doi:10.1152/ajpregu.00636.2007 PubMedCrossRef

Vechin FC, Libardi CA, Conceicao MS, Damas FR, Lixandrao ME, Berton RP, Tricoli VA, Roschel HA, Cavaglieri CR, Chacon-Mikahil MP, Ugrinowitsch C (2015) Comparisons between low-intensity resistance training with blood flow restriction and high-intensity resistance training on quadriceps muscle mass and strength in elderly. J Strength Cond Res 29(4):1071–1076. doi:10.1519/JSC.0000000000000703 PubMedCrossRef

Wakahara T, Ema R, Miyamoto N, Kawakami Y (2015) Increase in vastus lateralis aponeurosis width induced by resistance training: implications for a hypertrophic model of pennate muscle. Eur J Appl Physiol 115(2):309–316. doi:10.1007/s00421-014-3012-9 PubMedCrossRef

Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM (2007) Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85(4):1031–1040PubMed

Wilson GJ, Murphy AJ (1996) The use of isometric tests of muscular function in athletic assessment. Sports Med 22(1):19–37PubMedCrossRef

Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD (2014) Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr 99(1):86–95. doi:10.3945/ajcn.112.055517 PubMedCrossRef

Young HJ, Jenkins NT, Zhao Q, McCully KK (2015) Measurement of Intramuscular Fat by Muscle Echo Intensity. Muscle Nerve. doi:10.1002/mus.24656 PubMed

Title: Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling
Authors: Felipe Damas
Stuart M. Phillips
Manoel E. Lixandrão
Felipe C. Vechin
Cleiton A. Libardi
Hamilton Roschel
Valmor Tricoli
Carlos Ugrinowitsch
Publication date: 01-01-2016
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 1/2016
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-015-3243-4

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling

Abstract

Purpose

Methods

Result

Conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Result

Conclusion

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