Neuromuscular Electrical Stimulation in Muscular Adaptations in Exercise: A Narrative Review
الموضوعات :
1 - Assistant Professor, Department of Physical Education & Sport Sciences, Faculty of Humanities, Parand Branch, Islamic Azad University, Parand, Tehran, Iran
الکلمات المفتاحية: Neuromuscular Electrical Stimulation, Muscle Adaptations, Exercise, Performance, NMES,
ملخص المقالة :
Nowadays, sports science uses scientific methods and medical devices to assist people with any improvements in sports. Muscle adaptations have significantly benefited as a result of the use of these advanced devices. It has been shown that neuromuscular electrical stimulation (NMES) devices effectively improve muscle function. The use of NMES devices in exercise physiology shows that neuromuscular adaptation is a current research area in both athletes and non-athletes. This narrative review aims to address neuromuscular adaptations and describe neuromuscular changes based on research using NMES. Many researchers and sports trainers will benefit from the results of this article by better understanding neuromuscular adaptations. NMES training has been shown to be an effective way to improve muscle growth, maximum voluntary strength, neuronal drive, oxidative metabolism, and antioxidant defense systems. In addition, NMES is capable of regulating the homeostasis of muscle proteins and increasing oxidative enzyme activity. In animal models, it has also been shown to increase axonal outgrowth, fiber reinnervation, and motor axon regeneration. Various NMES methods may decrease age-related muscle atrophy and functional deterioration. The use of NMES, which is one of the most successful strategies for increasing athletic performance through neuromuscular adaptations, is one of the most promising areas of research.
المصادر:
1. Stillings D. Electrical stimulation for drop foot, 1772. Med Instrum. 1975 Nov-Dec;9(6):276-7. PMID: 1102876.
2. Lake DA. Neuromuscular electrical stimulation. An overview and its application in the treatment of sports injuries. Sports Med. 1992 May;13(5):320-36. doi: 10.2165/00007256-199213050-00003. PMID: 1565927.
3. Rahmati M, Gondin J, Malakoutinia F. Effects of Neuromuscular Electrical Stimulation on Quadriceps Muscle Strength and Mass in Healthy Young and Older Adults: A Scoping Review. Phys Ther. 2021 Sep 1;101(9). doi: 10.1093/ptj/pzab144. PMID: 34106246.
4. Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol. 2010 Sep;110(2):223-34. doi: 10.1007/s00421-010-1502-y. Epub 2010 May 15. PMID: 20473619.
5. Maffiuletti NA, Minetto MA, Farina D, Bottinelli R. Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol. 2011 Oct;111(10):2391-7. doi: 10.1007/s00421-011-2133-7. Epub 2011 Aug 25. PMID: 21866361.
6. Malone JK, Blake C, Caulfield BM. Neuromuscular electrical stimulation during recovery from exercise: a systematic review. J Strength Cond Res. 2014 Sep;28(9):2478-506. doi: 10.1519/JSC.0000000000000426. PMID: 24552796.
7. Cobb M. Timeline: exorcizing the animal spirits: Jan Swammerdam on nerve function. Nat Rev Neurosci. 2002 May;3(5):395-400. doi: 10.1038/nrn806. PMID: 11988778.
8. Gondin J, Cozzone PJ, Bendahan D. Is high-frequency neuromuscular electrical stimulation a suitable tool for muscle performance improvement in both healthy humans and athletes? Eur J Appl Physiol. 2011 Oct;111(10):2473-87. doi: 10.1007/s00421-011-2101-2. Epub 2011 Sep 10. PMID: 21909714.
9. Vincent R. From a laboratory to the wearables: a review on history and evolution of electrocardiogram. Iberoamerican Journal of Medicine; 2022 Sep 6;4(4):248–255. doi: 10.53986/ibjm.2022.0038.
10. Mondal S, Tazul Islam Md, Das A, Khandaker MU. Development of an Optimal Design and Subsequent Fabrication of an Electricity-Generating Ground Platform from Footstep. Lecture Notes on Data Engineering and Communications Technologies [Internet]. Springer Singapore; 2021 Dec 4;379–390. doi: 10.1007/978-981-16-6636-0_29.
11. Parent A. Duchenne De Boulogne: a pioneer in neurology and medical photography. Can J Neurol Sci. 2005 Aug;32(3):369-77. doi: 10.1017/s0317167100004315. PMID: 16225184.
12. Fénelon G. From Dreams to Hallucinations: Jean Lhermitte's Contribution to the Study of Peduncular Hallucinosis and the Dissociation of States. J Neuropsychiatry Clin Neurosci. 2022 Winter;34(1):16-29. doi: 10.1176/appi.neuropsych.20120314. Epub 2021 Oct 29. PMID: 34711070.
13. MERTON PA. Voluntary strength and fatigue. J Physiol. 1954 Mar 29;123(3):553-64. doi: 10.1113/jphysiol.1954.sp005070. PMID: 13152698.
14. Duchateau J, Le Bozec S, Hainaut K. Contributions of slow and fast muscles of triceps surae to a cyclic movement. Eur J Appl Physiol Occup Physiol. 1986;55(5):476-81. doi: 10.1007/BF00421640. PMID: 3769904.
15. Duchateau J, Hainaut K. Isometric or dynamic training: differential effects on mechanical properties of a human muscle. J Appl Physiol Respir Environ Exerc Physiol. 1984 Feb;56(2):296-301. doi: 10.1152/jappl.1984.56.2.296. PMID: 6706740.
16. Baudry S, Duchateau J. Postactivation potentiation in a human muscle: effect on the rate of torque development of tetanic and voluntary isometric contractions. J Appl Physiol (1985). 2007 Apr;102(4):1394-401. doi: 10.1152/japplphysiol.01254.2006. Epub 2007 Jan 4. PMID: 17204572.
17. Chan KM, Andres LP, Polykovskaya Y, Brown WF. The effects of training through high-frequency electrical stimulation on the physiological properties of single human thenar motor units. Muscle Nerve. 1999 Feb;22(2):186-95. doi: 10.1002/(sici)1097-4598(199902)22:2<186::aid-mus6>3.0.co;2-i. PMID: 10024131.
18. Stein RB, French AS, Mannard A, Yemm R. New methods for analysing motor function in man and animals. Brain Res. 1972 May 12;40(1):187-92. doi: 10.1016/0006-8993(72)90126-6. PMID: 5033795.
19. Hainaut K, Duchateau J, Desmedt JE. Differential effects on slow and fast motor units of different programs of brief daily muscle training in man. In: Desmedt JE, editor. Progress in Clinical Neurophysiology. Vol. 9. Basel: Karger; 1981. pp. 241–249.
20. Van Cutsem M, Duchateau J, Hainaut K. Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol. 1998 Nov 15;513 ( Pt 1)(Pt 1):295-305. doi: 10.1111/j.1469-7793.1998.295by.x. PMID: 9782179.
21. Lanza MB, Martins-Costa HC, De Souza CC, Lima FV, Diniz RCR, Chagas MH. Muscle volume vs. anatomical cross-sectional area: Different muscle assessment does not affect the muscle size-strength relationship. J Biomech. 2022 Feb; 132:110956. doi: 10.1016/j.jbiomech.2022.110956. Epub 2022 Jan 11. PMID: 35033973.
22. Narici MV, Hoppeler H, Kayser B, Landoni L, Claassen H, Gavardi C, Conti M, Cerretelli P. Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiol Scand. 1996 Jun;157(2):175-86. doi: 10.1046/j.1365-201X.1996.483230000.x. PMID: 8800357.
23. Komi PV. The Encyclopaedia of Sports Medicine, Neuromuscular Aspects of Sports Performance. Vol: 17 of The Encyclopaedia of Sports Medicine: John Wiley & Sons; 2011.
24. Schantz P, Randall-Fox E, Hutchison W, Tydén A, Astrand PO. Muscle fibre type distribution, muscle cross-sectional area and maximal voluntary strength in humans. Acta Physiol Scand. 1983 Feb;117(2):219-26. doi: 10.1111/j.1748-1716.1983.tb07200.x. PMID: 6223509.
25. Bartolomei S, Grillone G, Di Michele R, Cortesi M. A Comparison between Male and Female Athletes in Relative Strength and Power Performances. J Funct Morphol Kinesiol. 2021 Feb 9;6(1):17. doi: 10.3390/jfmk6010017. PMID: 33572280.
26. D'Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R, Rossi R, Moro G, Miotti D, Canepari M, Bottinelli R. Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol. 2006 Feb 1;570(Pt 3):611-27. doi: 10.1113/jphysiol.2005.101642. Epub 2005 Dec 8. PMID: 16339176.
27. Harber MP, Fry AC, Rubin MR, Smith JC, Weiss LW. Skeletal muscle and hormonal adaptations to circuit weight training in untrained men. Scand J Med Sci Sports. 2004 Jun;14(3):176-85. doi: 10.1111/j.1600-0838.2003.371.x. PMID: 15144358.
28. Gharahdaghi N, Phillips BE, Szewczyk NJ, Smith K, Wilkinson DJ, Atherton PJ. Links Between Testosterone, Oestrogen, and the Growth Hormone/Insulin-Like Growth Factor Axis and Resistance Exercise Muscle Adaptations. Front Physiol. 2021 Jan 15;11: 621226. doi: 10.3389/fphys.2020.621226. PMID: 33519525.
29. Sale D, MacDougall D. Specificity in strength training: a review for the coach and athlete. Can J Appl Sport Sci. 1981 Jun;6(2):87-92. PMID: 7016357.
30. Kadi F, Thornell LE. Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol. 2000 Feb;113(2):99-103. doi: 10.1007/s004180050012. PMID: 10766262.
31. Davies J, Parker DF, Rutherford OM, Jones DA. Changes in strength and cross sectional area of the elbow flexors as a result of isometric strength training. Eur J Appl Physiol Occup Physiol. 1988;57(6):667-70. doi: 10.1007/BF01075986. PMID: 3416850.
32. Alway SE, Grumbt WH, Stray-Gundersen J, Gonyea WJ. Effects of resistance training on elbow flexors of highly competitive bodybuilders. J Appl Physiol (1985). 1992 Apr;72(4):1512-21. doi: 10.1152/jappl.1992.72.4.1512. PMID: 1592744.
33. Tesch PA, Komi PV, Häkkinen K. Enzymatic adaptations consequent to long-term strength training. Int J Sports Med. 1987 Mar;8 Suppl 1:66-9. doi: 10.1055/s-2008-1025706. PMID: 2953691.
34. Aagaard P, Andersen JL, Dyhre-Poulsen P, Leffers AM, Wagner A, Magnusson SP, Halkjaer-Kristensen J, Simonsen EB. A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol. 2001 Jul 15;534(Pt. 2):613-23. doi: 10.1111/j.1469-7793. 2001.t01-1-00613.x. PMID: 11454977.
35. Canepari M, Rossi R, Pellegrino MA, Orrell RW, Cobbold M, Harridge S, Bottinelli R. Effects of resistance training on myosin function studied by the in vitro motility assay in young and older men. J Appl Physiol (1985). 2005 Jun;98(6):2390-5. doi: 10.1152/japplphysiol.01103.2004. Epub 2005 Jan 27. PMID: 15677736.
36. Malisoux L, Francaux M, Nielens H, Theisen D. Stretch-shortening cycle exercises: an effective training paradigm to enhance power output of human single muscle fibers. J Appl Physiol (1985). 2006 Mar;100(3):771-9. doi: 10.1152/japplphysiol.01027.2005. Epub 2005 Dec 1. PMID: 16322375.
37. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol (1985). 2007 Jan;102(1):368-73. doi: 10.1152/japplphysiol.00789.2006. Epub 2006 Oct 19. PMID: 17053104.
38. Sale DG, MacDougall JD, Alway SE, Sutton JR. Voluntary strength and muscle characteristics in untrained men and women and male bodybuilders. J Appl Physiol (1985). 1987 May;62(5):1786-93. doi: 10.1152/jappl.1987.62.5.1786. PMID: 3597252.
39. McCall GE, Byrnes WC, Dickinson A, Pattany PM, Fleck SJ. Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J Appl Physiol (1985). 1996 Nov;81(5):2004-12. doi: 10.1152/jappl.1996.81.5.2004. PMID: 8941522.
40. Pousson M, Van Hoecke J, Goubel F. Changes in elastic characteristics of human muscle induced by eccentric exercise. J Biomech. 1990;23(4):343-8. doi: 10.1016/0021-9290(90)90062-8. PMID: 2335532.
41. Cornu C, Almeida Silveira MI, Goubel F. Influence of plyometric training on the mechanical impedance of the human ankle joint. Eur J Appl Physiol Occup Physiol. 1997;76(3):282-8. doi: 10.1007/s004210050249. PMID: 9286610.
42. Ishikawa M, Komi PV, Finni T, Kuitunen S. Contribution of the tendinous tissue to force enhancement during stretch-shortening cycle exercise depends on the prestretch and concentric phase intensities. J Electromyogr Kinesiol. 2006 Oct;16(5):423-31. doi: 10.1016/j.jelekin.2005.08.006. Epub 2005 Nov 4. PMID: 16275136.
43. Duclay J, Robbe A, Pousson M, Martin A. Effect of angular velocity on soleus and medial gastrocnemius H-reflex during maximal concentric and eccentric muscle contraction. J Electromyogr Kinesiol. 2009 Oct;19(5):948-56. doi: 10.1016/j.jelekin.2008.04.011. Epub 2008 Jun 13. PMID: 18555699.
44. Magnusson SP, Kjaer M. Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. Eur J Appl Physiol. 2003 Nov;90(5-6):549-53. doi: 10.1007/s00421-003-0865-8. Epub 2003 Aug 5. PMID: 12905044.
45. Guo Y, E Phillips B, Atherton PJ, Piasecki M. Molecular and neural adaptations to neuromuscular electrical stimulation; Implications for ageing muscle. Mech Ageing Dev. 2021 Jan;193:111402. doi: 10.1016/j.mad.2020.111402. Epub 2020 Nov 13. PMID: 33189759.
46. 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. Electrical stimulation counteracts muscle decline in seniors. Front Aging Neurosci. 2014 Jul 24;6: 189. doi: 10.3389/fnagi.2014.00189. PMID: 25104935.
47. Enoka RM, Amiridis IG, Duchateau J. Electrical Stimulation of Muscle: Electrophysiology and Rehabilitation. Physiology (Bethesda). 2020 Jan 1;35(1):40-56. doi: 10.1152/physiol.00015.2019. PMID: 31799910.
48. HENNEMAN E, SOMJEN G, CARPENTER DO. FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS. J Neurophysiol. 1965 May; 28:560-80. doi: 10.1152/jn.1965.28.3.560. PMID: 14328454.
49. Swiecicka A, Piasecki M, Stashuk D, Jones D, Wu F, McPhee JS, Rutter MK. Relationship of Anabolic Hormones With Motor Unit Characteristics in Quadriceps Muscle in Healthy and Frail Aging Men. J Clin Endocrinol Metab. 2020 Jul 1;105(7): doi: 10.1210/clinem/dgaa100. PMID: 32133493.
50. Karlsen A, Cullum CK, Norheim KL, Scheel FU, Zinglersen AH, Vahlgren J, Schjerling P, Kjaer M, Mackey AL. Neuromuscular Electrical Stimulation Preserves Leg Lean Mass in Geriatric Patients. Med Sci Sports Exerc. 2020 Apr;52(4):773-784. doi: 10.1249/MSS.0000000000002191. PMID: 31688649.
51. Di Filippo ES, Mancinelli R, Marrone M, Doria C, Verratti V, Toniolo L, Dantas JL, Fulle S, Pietrangelo T. Neuromuscular electrical stimulation improves skeletal muscle regeneration through satellite cell fusion with myofibers in healthy elderly subjects. J Appl Physiol (1985). 2017 Sep 1;123(3):501-512. doi: 10.1152/japplphysiol.00855.2016. Epub 2017 Jun 1. PMID: 28572500.
52. Snijders T, Trommelen J, Kouw IWK, Holwerda AM, Verdijk LB, van Loon LJC. The Impact of Pre-sleep Protein Ingestion on the Skeletal Muscle Adaptive Response to Exercise in Humans: An Update. Front Nutr. 2019 Mar 6; 6:17. doi: 10.3389/fnut.2019.00017. PMID: 30895177.
53. Dirks ML, Wall BT, Kramer IF, Zorenc AH, Goessens JP, Gijsen AP, van Loon LJ. A single session of neuromuscular electrical stimulation does not augment postprandial muscle protein accretion. Am J Physiol Endocrinol Metab. 2016 Jul 1;311(1): E278-85. doi: 10.1152/ajpendo.00085.2016. Epub 2016 Jun 7. PMID: 27279248.
54. Wall BT, Dirks ML, Verdijk LB, Snijders T, Hansen D, Vranckx P, Burd NA, Dendale P, van Loon LJ. Neuromuscular electrical stimulation increases muscle protein synthesis in elderly type 2 diabetic men. Am J Physiol Endocrinol Metab. 2012 Sep 1;303(5): E614-23. doi: 10.1152/ajpendo.00138.2012. Epub 2012 Jun 26. PMID: 22739107.
1. Stillings D. Electrical stimulation for drop foot, 1772. Med Instrum. 1975 Nov-Dec;9(6):276-7. PMID: 1102876.
2. Lake DA. Neuromuscular electrical stimulation. An overview and its application in the treatment of sports injuries. Sports Med. 1992 May;13(5):320-36. doi: 10.2165/00007256-199213050-00003. PMID: 1565927.
3. Rahmati M, Gondin J, Malakoutinia F. Effects of Neuromuscular Electrical Stimulation on Quadriceps Muscle Strength and Mass in Healthy Young and Older Adults: A Scoping Review. Phys Ther. 2021 Sep 1;101(9). doi: 10.1093/ptj/pzab144. PMID: 34106246.
4. Maffiuletti NA. Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol. 2010 Sep;110(2):223-34. doi: 10.1007/s00421-010-1502-y. Epub 2010 May 15. PMID: 20473619.
5. Maffiuletti NA, Minetto MA, Farina D, Bottinelli R. Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues. Eur J Appl Physiol. 2011 Oct;111(10):2391-7. doi: 10.1007/s00421-011-2133-7. Epub 2011 Aug 25. PMID: 21866361.
6. Malone JK, Blake C, Caulfield BM. Neuromuscular electrical stimulation during recovery from exercise: a systematic review. J Strength Cond Res. 2014 Sep;28(9):2478-506. doi: 10.1519/JSC.0000000000000426. PMID: 24552796.
7. Cobb M. Timeline: exorcizing the animal spirits: Jan Swammerdam on nerve function. Nat Rev Neurosci. 2002 May;3(5):395-400. doi: 10.1038/nrn806. PMID: 11988778.
8. Gondin J, Cozzone PJ, Bendahan D. Is high-frequency neuromuscular electrical stimulation a suitable tool for muscle performance improvement in both healthy humans and athletes? Eur J Appl Physiol. 2011 Oct;111(10):2473-87. doi: 10.1007/s00421-011-2101-2. Epub 2011 Sep 10. PMID: 21909714.
9. Vincent R. From a laboratory to the wearables: a review on history and evolution of electrocardiogram. Iberoamerican Journal of Medicine; 2022 Sep 6;4(4):248–255. doi: 10.53986/ibjm.2022.0038.
10. Mondal S, Tazul Islam Md, Das A, Khandaker MU. Development of an Optimal Design and Subsequent Fabrication of an Electricity-Generating Ground Platform from Footstep. Lecture Notes on Data Engineering and Communications Technologies [Internet]. Springer Singapore; 2021 Dec 4;379–390. doi: 10.1007/978-981-16-6636-0_29.
11. Parent A. Duchenne De Boulogne: a pioneer in neurology and medical photography. Can J Neurol Sci. 2005 Aug;32(3):369-77. doi: 10.1017/s0317167100004315. PMID: 16225184.
12. Fénelon G. From Dreams to Hallucinations: Jean Lhermitte's Contribution to the Study of Peduncular Hallucinosis and the Dissociation of States. J Neuropsychiatry Clin Neurosci. 2022 Winter;34(1):16-29. doi: 10.1176/appi.neuropsych.20120314. Epub 2021 Oct 29. PMID: 34711070.
13. MERTON PA. Voluntary strength and fatigue. J Physiol. 1954 Mar 29;123(3):553-64. doi: 10.1113/jphysiol.1954.sp005070. PMID: 13152698.
14. Duchateau J, Le Bozec S, Hainaut K. Contributions of slow and fast muscles of triceps surae to a cyclic movement. Eur J Appl Physiol Occup Physiol. 1986;55(5):476-81. doi: 10.1007/BF00421640. PMID: 3769904.
15. Duchateau J, Hainaut K. Isometric or dynamic training: differential effects on mechanical properties of a human muscle. J Appl Physiol Respir Environ Exerc Physiol. 1984 Feb;56(2):296-301. doi: 10.1152/jappl.1984.56.2.296. PMID: 6706740.
16. Baudry S, Duchateau J. Postactivation potentiation in a human muscle: effect on the rate of torque development of tetanic and voluntary isometric contractions. J Appl Physiol (1985). 2007 Apr;102(4):1394-401. doi: 10.1152/japplphysiol.01254.2006. Epub 2007 Jan 4. PMID: 17204572.
17. Chan KM, Andres LP, Polykovskaya Y, Brown WF. The effects of training through high-frequency electrical stimulation on the physiological properties of single human thenar motor units. Muscle Nerve. 1999 Feb;22(2):186-95. doi: 10.1002/(sici)1097-4598(199902)22:2<186::aid-mus6>3.0.co;2-i. PMID: 10024131.
18. Stein RB, French AS, Mannard A, Yemm R. New methods for analysing motor function in man and animals. Brain Res. 1972 May 12;40(1):187-92. doi: 10.1016/0006-8993(72)90126-6. PMID: 5033795.
19. Hainaut K, Duchateau J, Desmedt JE. Differential effects on slow and fast motor units of different programs of brief daily muscle training in man. In: Desmedt JE, editor. Progress in Clinical Neurophysiology. Vol. 9. Basel: Karger; 1981. pp. 241–249.
20. Van Cutsem M, Duchateau J, Hainaut K. Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol. 1998 Nov 15;513 ( Pt 1)(Pt 1):295-305. doi: 10.1111/j.1469-7793.1998.295by.x. PMID: 9782179.
21. Lanza MB, Martins-Costa HC, De Souza CC, Lima FV, Diniz RCR, Chagas MH. Muscle volume vs. anatomical cross-sectional area: Different muscle assessment does not affect the muscle size-strength relationship. J Biomech. 2022 Feb; 132:110956. doi: 10.1016/j.jbiomech.2022.110956. Epub 2022 Jan 11. PMID: 35033973.
22. Narici MV, Hoppeler H, Kayser B, Landoni L, Claassen H, Gavardi C, Conti M, Cerretelli P. Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiol Scand. 1996 Jun;157(2):175-86. doi: 10.1046/j.1365-201X.1996.483230000.x. PMID: 8800357.
23. Komi PV. The Encyclopaedia of Sports Medicine, Neuromuscular Aspects of Sports Performance. Vol: 17 of The Encyclopaedia of Sports Medicine: John Wiley & Sons; 2011.
24. Schantz P, Randall-Fox E, Hutchison W, Tydén A, Astrand PO. Muscle fibre type distribution, muscle cross-sectional area and maximal voluntary strength in humans. Acta Physiol Scand. 1983 Feb;117(2):219-26. doi: 10.1111/j.1748-1716.1983.tb07200.x. PMID: 6223509.
25. Bartolomei S, Grillone G, Di Michele R, Cortesi M. A Comparison between Male and Female Athletes in Relative Strength and Power Performances. J Funct Morphol Kinesiol. 2021 Feb 9;6(1):17. doi: 10.3390/jfmk6010017. PMID: 33572280.
26. D'Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R, Rossi R, Moro G, Miotti D, Canepari M, Bottinelli R. Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol. 2006 Feb 1;570(Pt 3):611-27. doi: 10.1113/jphysiol.2005.101642. Epub 2005 Dec 8. PMID: 16339176.
27. Harber MP, Fry AC, Rubin MR, Smith JC, Weiss LW. Skeletal muscle and hormonal adaptations to circuit weight training in untrained men. Scand J Med Sci Sports. 2004 Jun;14(3):176-85. doi: 10.1111/j.1600-0838.2003.371.x. PMID: 15144358.
28. Gharahdaghi N, Phillips BE, Szewczyk NJ, Smith K, Wilkinson DJ, Atherton PJ. Links Between Testosterone, Oestrogen, and the Growth Hormone/Insulin-Like Growth Factor Axis and Resistance Exercise Muscle Adaptations. Front Physiol. 2021 Jan 15;11: 621226. doi: 10.3389/fphys.2020.621226. PMID: 33519525.
29. Sale D, MacDougall D. Specificity in strength training: a review for the coach and athlete. Can J Appl Sport Sci. 1981 Jun;6(2):87-92. PMID: 7016357.
30. Kadi F, Thornell LE. Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol. 2000 Feb;113(2):99-103. doi: 10.1007/s004180050012. PMID: 10766262.
31. Davies J, Parker DF, Rutherford OM, Jones DA. Changes in strength and cross sectional area of the elbow flexors as a result of isometric strength training. Eur J Appl Physiol Occup Physiol. 1988;57(6):667-70. doi: 10.1007/BF01075986. PMID: 3416850.
32. Alway SE, Grumbt WH, Stray-Gundersen J, Gonyea WJ. Effects of resistance training on elbow flexors of highly competitive bodybuilders. J Appl Physiol (1985). 1992 Apr;72(4):1512-21. doi: 10.1152/jappl.1992.72.4.1512. PMID: 1592744.
33. Tesch PA, Komi PV, Häkkinen K. Enzymatic adaptations consequent to long-term strength training. Int J Sports Med. 1987 Mar;8 Suppl 1:66-9. doi: 10.1055/s-2008-1025706. PMID: 2953691.
34. Aagaard P, Andersen JL, Dyhre-Poulsen P, Leffers AM, Wagner A, Magnusson SP, Halkjaer-Kristensen J, Simonsen EB. A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol. 2001 Jul 15;534(Pt. 2):613-23. doi: 10.1111/j.1469-7793. 2001.t01-1-00613.x. PMID: 11454977.
35. Canepari M, Rossi R, Pellegrino MA, Orrell RW, Cobbold M, Harridge S, Bottinelli R. Effects of resistance training on myosin function studied by the in vitro motility assay in young and older men. J Appl Physiol (1985). 2005 Jun;98(6):2390-5. doi: 10.1152/japplphysiol.01103.2004. Epub 2005 Jan 27. PMID: 15677736.
36. Malisoux L, Francaux M, Nielens H, Theisen D. Stretch-shortening cycle exercises: an effective training paradigm to enhance power output of human single muscle fibers. J Appl Physiol (1985). 2006 Mar;100(3):771-9. doi: 10.1152/japplphysiol.01027.2005. Epub 2005 Dec 1. PMID: 16322375.
37. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol (1985). 2007 Jan;102(1):368-73. doi: 10.1152/japplphysiol.00789.2006. Epub 2006 Oct 19. PMID: 17053104.
38. Sale DG, MacDougall JD, Alway SE, Sutton JR. Voluntary strength and muscle characteristics in untrained men and women and male bodybuilders. J Appl Physiol (1985). 1987 May;62(5):1786-93. doi: 10.1152/jappl.1987.62.5.1786. PMID: 3597252.
39. McCall GE, Byrnes WC, Dickinson A, Pattany PM, Fleck SJ. Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J Appl Physiol (1985). 1996 Nov;81(5):2004-12. doi: 10.1152/jappl.1996.81.5.2004. PMID: 8941522.
40. Pousson M, Van Hoecke J, Goubel F. Changes in elastic characteristics of human muscle induced by eccentric exercise. J Biomech. 1990;23(4):343-8. doi: 10.1016/0021-9290(90)90062-8. PMID: 2335532.
41. Cornu C, Almeida Silveira MI, Goubel F. Influence of plyometric training on the mechanical impedance of the human ankle joint. Eur J Appl Physiol Occup Physiol. 1997;76(3):282-8. doi: 10.1007/s004210050249. PMID: 9286610.
42. Ishikawa M, Komi PV, Finni T, Kuitunen S. Contribution of the tendinous tissue to force enhancement during stretch-shortening cycle exercise depends on the prestretch and concentric phase intensities. J Electromyogr Kinesiol. 2006 Oct;16(5):423-31. doi: 10.1016/j.jelekin.2005.08.006. Epub 2005 Nov 4. PMID: 16275136.
43. Duclay J, Robbe A, Pousson M, Martin A. Effect of angular velocity on soleus and medial gastrocnemius H-reflex during maximal concentric and eccentric muscle contraction. J Electromyogr Kinesiol. 2009 Oct;19(5):948-56. doi: 10.1016/j.jelekin.2008.04.011. Epub 2008 Jun 13. PMID: 18555699.
44. Magnusson SP, Kjaer M. Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. Eur J Appl Physiol. 2003 Nov;90(5-6):549-53. doi: 10.1007/s00421-003-0865-8. Epub 2003 Aug 5. PMID: 12905044.
45. Guo Y, E Phillips B, Atherton PJ, Piasecki M. Molecular and neural adaptations to neuromuscular electrical stimulation; Implications for ageing muscle. Mech Ageing Dev. 2021 Jan;193:111402. doi: 10.1016/j.mad.2020.111402. Epub 2020 Nov 13. PMID: 33189759.
46. 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. Electrical stimulation counteracts muscle decline in seniors. Front Aging Neurosci. 2014 Jul 24;6: 189. doi: 10.3389/fnagi.2014.00189. PMID: 25104935.
47. Enoka RM, Amiridis IG, Duchateau J. Electrical Stimulation of Muscle: Electrophysiology and Rehabilitation. Physiology (Bethesda). 2020 Jan 1;35(1):40-56. doi: 10.1152/physiol.00015.2019. PMID: 31799910.
48. HENNEMAN E, SOMJEN G, CARPENTER DO. FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS. J Neurophysiol. 1965 May; 28:560-80. doi: 10.1152/jn.1965.28.3.560. PMID: 14328454.
49. Swiecicka A, Piasecki M, Stashuk D, Jones D, Wu F, McPhee JS, Rutter MK. Relationship of Anabolic Hormones With Motor Unit Characteristics in Quadriceps Muscle in Healthy and Frail Aging Men. J Clin Endocrinol Metab. 2020 Jul 1;105(7): doi: 10.1210/clinem/dgaa100. PMID: 32133493.
50. Karlsen A, Cullum CK, Norheim KL, Scheel FU, Zinglersen AH, Vahlgren J, Schjerling P, Kjaer M, Mackey AL. Neuromuscular Electrical Stimulation Preserves Leg Lean Mass in Geriatric Patients. Med Sci Sports Exerc. 2020 Apr;52(4):773-784. doi: 10.1249/MSS.0000000000002191. PMID: 31688649.
51. Di Filippo ES, Mancinelli R, Marrone M, Doria C, Verratti V, Toniolo L, Dantas JL, Fulle S, Pietrangelo T. Neuromuscular electrical stimulation improves skeletal muscle regeneration through satellite cell fusion with myofibers in healthy elderly subjects. J Appl Physiol (1985). 2017 Sep 1;123(3):501-512. doi: 10.1152/japplphysiol.00855.2016. Epub 2017 Jun 1. PMID: 28572500.
52. Snijders T, Trommelen J, Kouw IWK, Holwerda AM, Verdijk LB, van Loon LJC. The Impact of Pre-sleep Protein Ingestion on the Skeletal Muscle Adaptive Response to Exercise in Humans: An Update. Front Nutr. 2019 Mar 6; 6:17. doi: 10.3389/fnut.2019.00017. PMID: 30895177.
53. Dirks ML, Wall BT, Kramer IF, Zorenc AH, Goessens JP, Gijsen AP, van Loon LJ. A single session of neuromuscular electrical stimulation does not augment postprandial muscle protein accretion. Am J Physiol Endocrinol Metab. 2016 Jul 1;311(1): E278-85. doi: 10.1152/ajpendo.00085.2016. Epub 2016 Jun 7. PMID: 27279248.
54. Wall BT, Dirks ML, Verdijk LB, Snijders T, Hansen D, Vranckx P, Burd NA, Dendale P, van Loon LJ. Neuromuscular electrical stimulation increases muscle protein synthesis in elderly type 2 diabetic men. Am J Physiol Endocrinol Metab. 2012 Sep 1;303(5): E614-23. doi: 10.1152/ajpendo.00138.2012. Epub 2012 Jun 26. PMID: 22739107.
