Top

European Journal of Applied Physiology

Published in:

19-10-2022 | Original Article

Effect of electromyostimulation training on intramuscular fat accumulation determined by ultrasonography in older adults

Authors: Maya Hioki, Hiroko Takahashi, Akira Saito, Mizuka Imai, Hideki Yasuda

Published in: European Journal of Applied Physiology | Issue 2/2023

Abstract

Purpose

Electromyostimulation (EMS) induces a short-term change in muscle metabolism, and EMS training induces long-term improvements of muscle atrophy and function. However, the effects of EMS training on intramuscular fat in older adults are still poorly known. The purpose of this study was to examine whether the intramuscular fat index and biochemical parameters change with EMS training of the quadriceps femoris muscles in older adults.

Methods

Nineteen non-obese older men and women performed EMS training of the quadriceps femoris for 12 weeks (3 times/week; single session for 30 min). The intramuscular fat content index was estimated by echo intensity of the vastus lateralis and rectus femoris muscles on ultrasonography, and muscle thickness was also measured. Muscle strength was assessed as the maximal voluntary contraction during isometric knee extension. Echo intensity, muscle thickness, and muscle strength were measured before and after EMS training. A rested/fasting blood samples were collected before and after EMS training for measuring plasma glucose, insulin, free fatty acid, triglyceride, and interleukin-6 concentrations. To examine the acute effect of a single-EMS session on biochemical parameters, blood samples were taken before and after the EMS session.

Results

EMS training did not significantly change echo intensity in muscles, muscle thickness, muscle strength, or biochemical parameters. Regarding the acute effect on blood lipid concentrations, a single-EMS session increased free fatty acid and glucose concentrations.

Conclusion

EMS sessions had an acute effect of increasing free fatty acid and glucose concentrations, but EMS training intervention did not improve intramuscular fat content.

Available only for authorised users

Aagaard P, Suetta C, Caserotti P, Magnusson SP, Kjaer M (2010) Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Scand J Med Sci Sports 20(1):49–64. https://doi.org/10.1111/j.1600-0838.2009.01084.xCrossRef

Abdollahi A, Dowden BN, Buhman KK, Zembroski AS, Henderson GC (2022) Albumin knockout mice exhibit reduced plasma free fatty acid concentration and enhanced insulin sensitivity. Physiol Rep 10(5):e15161. https://doi.org/10.14814/phy2.15161CrossRef

Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74(2):532–537CrossRef

Akima H, Kano Y, Enomoto Y, Ishizu M, Okada M, Oishi Y, Katsuta S, Kuno S (2001a) Muscle function in 164 men and women aged 20–84 yr. Med Sci Sports Exerc 33:220–226CrossRef

Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y, Gunji A, Fukunaga T (2001b) Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand 172:269–278CrossRef

Bickel CS, Slade J, Mahoney E, Haddad F, Dudley GA (1985) Adams GR (2005) time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise. J Appl Physiol 98(2):482–488. https://doi.org/10.1152/japplphysiol.00895.2004CrossRef

Boesch C, Machann J, Vermathen P, Schick F (2006) Role of proton MR for the study of muscle lipid metabolism. NMR Biomed 19:968–988CrossRef

Caggiano E, Emrey T, Shirley S, Craik RL (1994) Effects of electrical stimulation or voluntary contraction for strengthening the quadriceps femoris muscles in an aged male population. J Orthop Sports Phys Ther 20(1):22–28. https://doi.org/10.2519/jospt.1994.20.1.22CrossRef

Canepari M, Rossi R, Pellegrino MA, Orrell RW, Cobbold M, Harridge S, Bottinelli R (2005) Effects of resistance training on myosin function studied by the in vitro motility assay in young and older men. J Appl Physiol 98(6):2390–2395. https://doi.org/10.1152/japplphysiol.01103.2004CrossRef

Cartee GD, Hepple RT, Bamman MM, Zierath JR (2016) Exercise promotes healthy aging of skeletal muscle. Cell Metab 23(6):1034–1047. https://doi.org/10.1016/j.cmet.2016.05.007CrossRef

Caserotti P, Aagaard P, Puggaard L (2008) Changes in power and force generation during coupled eccentric-concentric versus concentric muscle contraction with training and aging. Eur J Appl Physiol 103(2):151–161. https://doi.org/10.1007/s00421-008-0678-xCrossRef

Chee C, Shannon CE, Burns A, Selby AL, Wilkinson D, Smith K, Greenhaff PL, Stephens FB (2016) Relative contribution of intramyocellular lipid to whole-body fat oxidation is reduced with age but subsarcolemmal lipid accumulation and insulin resistance are only associated with overweight individuals. Diabetes 65(4):840–850. https://doi.org/10.2337/db15-1383CrossRef

Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Academic Press, New York

Crane JD, Devries MD, Safdar A, Hamadeh MJ, Tarnopolsky MA (2010) The effect of aging on human skeletal muscle mitochondrial and intramyocellular lipid ultrastructure. J Gerontol A Biol Sci Med Sci 65A:119–128CrossRef

Egan B, Zierath JR (2013) Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17(2):162–184. https://doi.org/10.1016/j.cmet.2012.12.012CrossRef

Galvan MJ, Sanchez MJ, McAinch AJ, Covington JD, Boyle JB, Bajpeyi S (2022) Four weeks of electrical stimulation improves glucose tolerance in a sedentary overweight or obese hispanic population. Endocr Connect. https://doi.org/10.1530/ec-21-0533CrossRef

Gauthier JM, Theriault R, Theriault G, Gelinas Y, Simoneau JA (1992) Electrical stimulation-induced changes in skeletal muscle enzymes of men and women. Med Sci Sports Exerc 24(11):1252–1256

Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, Pellegrino MA, Bottinelli R (2011) Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 110(2):433–450. https://doi.org/10.1152/japplphysiol.00914.2010CrossRef

Gorgey AS, Shepherd C (2010) Skeletal muscle hypertrophy and decreased intramuscular fat after unilateral resistance training in spinal cord injury: case report. J Spinal Cord Med 33(1):90–95CrossRef

Gorgey AS, Mather KJ, Cupp HR, Gater DR (2012) Effects of resistance training on adiposity and metabolism after spinal cord injury. Med Sci Sports Exerc 44(1):165–174. https://doi.org/10.1249/MSS.0b013e31822672aaCrossRef

Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Gater DR (2015) The effects of electrical stimulation on body composition and metabolic profile after spinal cord injury - Part II. J Spinal Cord Med 38(1):23–37. https://doi.org/10.1179/2045772314y.0000000244CrossRef

Hamada T, Sasaki H, Hayashi T, Moritani T, Nakao K (2003) Enhancement of whole body glucose uptake during and after human skeletal muscle low-frequency electrical stimulation. J Appl Physiol 94(6):2107–2112. https://doi.org/10.1152/japplphysiol.00486.2002CrossRef

Hioki M, Kanehira N, Koike T, Saito A, Takahashi H, Shimaoka K, Sakakibara H, Oshida Y, Akima H (2016) Associations of intramyocellular lipid in vastus lateralis and biceps femoris with blood free fatty acid and muscle strength differ between young and elderly adults. Clin Physiol Funct Imaging 36(6):457–463. https://doi.org/10.1111/cpf.12250CrossRef

Hioki M, Kanehira N, Koike T, Saito A, Takahashi H, Shimaoka K, Sakakibara H, Oshida Y, Akima H (2019) Relationship between physical activity and intramyocellular lipid content is different between young and older adults. Eur J Appl Physiol 119(1):113–122. https://doi.org/10.1007/s00421-018-4005-xCrossRef

Hioki M, Kanehira N, Koike T, Saito A, Shimaoka K, Sakakibara H, Oshida Y, Akima H (2020) Age-related changes in muscle volume and intramuscular fat content in quadriceps femoris and hamstrings. Exp Gerontol 132:110834. https://doi.org/10.1016/j.exger.2020.110834CrossRef

Hioki M, Kanehira N, Koike T, Saito A, Takahashi H, Shimaoka K, Sakakibara H, Oshida Y, Akima H (2021) Effect of electromyostimulation on intramyocellular lipids of the vastus lateralis in older adults: a randomized controlled trial. BMC Musculoskelet Disord 22(1):569. https://doi.org/10.1186/s12891-021-04456-6CrossRef

Jensen MD (2003) Fate of fatty acids at rest and during exercise: regulatory mechanisms. Acta Physiol Scand 178(4):385–390. https://doi.org/10.1046/j.1365-201X.2003.01167.xCrossRef

Kern H, Barberi L, Löfler S, Sbardella S, Burggraf S, Fruhmann H, Carraro U, Mosole S, Sarabon N, Vogelauer M, Mayr W, Krenn M, Cvecka J, Romanello V, Pietrangelo L, Protasi F, Sandri M, Zampieri S, Musaro A (2014) Electrical stimulation counteracts muscle decline in seniors. Frontiers Aging Neurosci 6:189. https://doi.org/10.3389/fnagi.2014.00189CrossRef

Kohrt WM, Holloszy JO (1995) Loss of skeletal muscle mass with aging: effect on glucose tolerance. J Gerontol A Biol Sci Med Sci 50:S68-72

Kudo N, Nishide R, Mizutani M, Ogawa S, Tanimura S (2021) Association between the type of physical activity and metabolic syndrome in middle-aged and older adult residents of a semi-mountainous area in Japan. Environ Health Prev Med 26(1):46. https://doi.org/10.1186/s12199-021-00949-xCrossRef

Kumahara H, Schutz Y, Ayabe M, Yoshioka M, Yoshitake Y, Shindo M, Ishii K, Tanaka H (2004) The use of uniaxial accelerometry for the assessment of physical-activity-related energy expenditure: a validation study against whole-body indirect calorimetry. Br J Nutr 91(2):235–243. https://doi.org/10.1079/bjn20031033CrossRef

Langeard A, Bigot L, Chastan N, Gauthier A (2017) Does neuromuscular electrical stimulation training of the lower limb have functional effects on the elderly?: a systematic review. Exp Gerontol 91:88–98. https://doi.org/10.1016/j.exger.2017.02.070CrossRef

Lexell J, Taylor CC, Sjöström M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84(2–3):275–294. https://doi.org/10.1016/0022-510x(88)90132-3CrossRef

Lexell J (1995) Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50 Spec No:11-16. doi:https://doi.org/10.1093/gerona/50a.special_issue.11

Loher H, Kreis R, Boesch C, Christ E (2016) The flexibility of ectopic lipids. Int J Mol Sci. https://doi.org/10.3390/ijms17091554CrossRef

Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110(2):223–234. https://doi.org/10.1007/s00421-010-1502-yCrossRef

Maffiuletti NA, Dugnani S, Folz M, Di Pierno E, Mauro F (2002) Effect of combined electrostimulation and plyometric training on vertical jump height. Med Sci Sports Exerc 34(10):1638–1644. https://doi.org/10.1097/00005768-200210000-00016CrossRef

Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28(7):412–419CrossRef

Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, Fialka-Moser V, Quittan M, Pette D (2003) Functional and biochemical properties of chronically stimulated human skeletal muscle. Eur J Appl Physiol 89(2):202–208. https://doi.org/10.1007/s00421-003-0792-8CrossRef

Perez M, Lucia A, Rivero JL, Serrano AL, Calbet JA, Delgado MA, Chicharro JL (2002) Effects of transcutaneous short-term electrical stimulation on m. vastus lateralis characteristics of healthy young men. Pflugers Arch 443(5–6):866–874. https://doi.org/10.1007/s00424-001-0769-6CrossRef

Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, Wolfe RR (1993) Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol 265(3 Pt 1):E380-391

Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF (2002) Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 83(12):1703–1707. https://doi.org/10.1053/apmr.2002.36399CrossRef

Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Ivey FM (2011) Atrophy and intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 25(9):865–872. https://doi.org/10.1177/1545968311408920CrossRef

Sillen MJ, Franssen FM, Gosker HR, Wouters EF, Spruit MA (2013) Metabolic and structural changes in lower-limb skeletal muscle following neuromuscular electrical stimulation: a systematic review. PLoS ONE 8(9):e69391. https://doi.org/10.1371/journal.pone.0069391CrossRef

Suh SH, Paik IY, Jacobs K (2007) Regulation of blood glucose homeostasis during prolonged exercise. Mol Cells 23(3):272–279

Theriault R, Theriault G, Simoneau JA (1994) Human skeletal muscle adaptation in response to chronic low-frequency electrical stimulation. J Appl Physiol 77(4):1885–1889CrossRef

Theriault R, Boulay MR, Theriault G, Simoneau JA (1996) Electrical stimulation-induced changes in performance and fiber type proportion of human knee extensor muscles. Eur J Appl Physiol Occup Physiol 74(4):311–317CrossRef

Tsintzas K, Stephens FB, Snijders T, Wall BT, Cooper S, Mallinson J, Verdijk LB, van Loon LJC (2017) Intramyocellular lipid content and lipogenic gene exprssion responses following a single bout of resistance type exercise differ between young and older men. Exp Gerontol 93:36–45. https://doi.org/10.1016/j.exger.2017.03.018CrossRef

Verdijk LB, Gleeson BG, Jonkers RA, Meijer K, Savelberg HH, Dendale P, van Loon LJ (2009) Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J Gerontol A Biol Sci Med Sci 64(3):332–339. https://doi.org/10.1093/gerona/gln050CrossRef

Wang Q, Zhang X, Fang L, Guan Q, Gao L, Li Q (2018) Physical activity patterns and risk of type 2 diabetes and metabolic syndrome in middle-aged and elderly northern Chinese adults. J Diabetes Res 2018:7198274. https://doi.org/10.1155/2018/7198274CrossRef

Wittmann K, Sieber C, von Stengel S, Kohl M, Freiberger E, Jakob F, Lell M, Engelke K, Kemmler W (2016) Impact of whole body electromyostimulation on cardiometabolic risk factors in older women with sarcopenic obesity: the randomized controlled FORMOsA-sarcopenic obesity study. Clin Interv Aging 11:1697–1706. https://doi.org/10.2147/cia.S116430CrossRef

Title: Effect of electromyostimulation training on intramuscular fat accumulation determined by ultrasonography in older adults
Authors: Maya Hioki
Hiroko Takahashi
Akira Saito
Mizuka Imai
Hideki Yasuda
Publication date: 19-10-2022
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 2/2023
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-022-05074-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Effect of electromyostimulation training on intramuscular fat accumulation determined by ultrasonography in older adults

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 2/2023

Robust arm and leg muscle adaptation to training despite ACE inhibition: a randomized placebo-controlled trial

Time to retire the notion that local and whole-body exercise thresholds are mechanistically linked?

Minimal adaptation of the molecular regulators of mitochondrial dynamics in response to unilateral limb immobilisation and retraining in middle-aged men

The effects of α-lactalbumin supplementation and handgrip contraction on soleus motoneuron excitability

Adding heat stress to repeated-sprint training in hypoxia does not enhance performance improvements in canoe/kayak athletes

Knee position sense and knee flexor neuromuscular function are similarly altered after two submaximal eccentric bouts