Recovery from muscle weakness by exercise and FES: lessons from Masters, active or sedentary seniors and SCI patients

Abstract

Many factors contribute to the decline of skeletal muscle that occurs as we age. This is a reality that we may combat, but not prevent because it is written into our genome. The series of records from World Master Athletes reveals that skeletal muscle power begins to decline at the age of 30 years and continues, almost linearly, to zero at the age of 110 years. Here we discuss evidence that denervation contributes to the atrophy and slowness of aged muscle. We compared muscle from lifelong active seniors to that of sedentary elderly people and found that the sportsmen have more muscle bulk and slow fiber type groupings, providing evidence that physical activity maintains slow motoneurons which reinnervate muscle fibers. Further, accelerated muscle atrophy/degeneration occurs with irreversible Conus and Cauda Equina syndrome, a spinal cord injury in which the human leg muscles may be permanently disconnected from the nervous system with complete loss of muscle fibers within 5–8 years. We used histological morphometry and Muscle Color Computed Tomography to evaluate muscle from these peculiar persons and reveal that contraction produced by home-based Functional Electrical Stimulation (h-bFES) recovers muscle size and function which is reversed if h-bFES is discontinued. FES also reverses muscle atrophy in sedentary seniors and modulates mitochondria in horse muscles. All together these observations indicate that FES modifies muscle fibers by increasing contractions per day. Thus, FES should be considered in critical care units, rehabilitation centers and nursing facilities when patients are unable or reluctant to exercise.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 1.

    Lømo T (2014) The response of denervated muscle to long-term stimulation (1985, revisited here in 2014). Eur J Transl Myol Basic Appl Myol 24:13–19

    Google Scholar 

  2. 2.

    Mitchell WK, Williams J, Atherton P et al (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3:260. doi:10.3389/fphys.2012.00260

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Hepple RT, Rice CL (2015) Innervation and neuromuscular control in ageing skeletal muscle. J Physiol. doi:10.1113/JP270561

    PubMed  PubMed Central  Google Scholar 

  4. 4.

    Gava P, Kern H, Carraro U (2015) Age-associated power decline from running, jumping, and throwing male masters world records. Exp Aging Res 41:115–135. doi:10.1080/0361073X.2015.1001648

    Article  PubMed  Google Scholar 

  5. 5.

    Gordon T, English AW (2016) Strategies to promote peripheral nerve regeneration: electrical stimulation and/or exercise. Eur J Neurosci 43:336–350. doi:10.1111/ejn.13005

    Article  PubMed  Google Scholar 

  6. 6.

    Hill AV (1925) The physiological basis of athletic records. Sci Month 2:409–428

    Google Scholar 

  7. 7.

    Mosole S, Rossini K, Kern H et al (2013) Significant increase of vastus lateralis reinnervation in 70-year sportsmen with a lifelong history of high-level exercise. Eur J Transl Myol Basic Appl Myol 23:117–122

    Google Scholar 

  8. 8.

    Mosole S, Carraro U, Kern H et al (2014) Long-term high-level exercise promotes muscle reinnervation with age. J Neuropathol Exp Neurol 73:284–294. doi:10.1097/NEN.0000000000000032

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Stålberg E, Fawcett PR (1982) Macro EMG in healthy subjects of different ages. J Neurol Neurosurg Psychiatry 45:870–878

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95:1717–1727. doi:10.1152/japplphysiol.00347.2003

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Lexell J, Downham DY (1991) The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol 81:377–381

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Ling SM, Conwit RA, Ferrucci L et al (2009) Age-associated changes in motor unit physiology: observations from the Baltimore Longitudinal Study of Aging. Arch Phys Med Rehabil 90:1237–1240

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of 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 84:275–294

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Doherty TJ, Vandervoort AA, Taylor AW et al (1985) Effects of motor unit losses on strength in older men and women. J Appl Physiol 1993:868–874

    Google Scholar 

  15. 15.

    Payne AM, Delbono O (2004) Neurogenesis of excitation-contraction uncoupling in aging skeletal muscle. Exerc Sport Sci Rev 32:36–40

    Article  PubMed  Google Scholar 

  16. 16.

    Delbono O (2003) Neural control of aging skeletal muscle. Aging Cell 2:21–29

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Zampieri S, Pietrangelo L, Loefler S et al (2015) Lifelong physical exercise delays age-associated skeletal muscle decline. J Gerontol A Biol Sci Med Sci 70:163–173. doi:10.1093/gerona/glu006

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Messi ML, Li T, Wang ZM et al (2015) Resistance training enhances skeletal muscle innervation without modifying the number of satellite cells or their myofiber association in obese older adults. J Gerontol A Biol Sci Med Sci. pii:glv176

    Google Scholar 

  19. 19.

    Dow DE, Dennis RG, Faulkner JA (2005) Electrical stimulation attenuates denervation and age-related atrophy in extensor digitorum longus muscles of old rats. J Gerontol A Biol Sci Med Sci 60:416–424

    Article  PubMed  Google Scholar 

  20. 20.

    Hennig R, Lømo T (1985) Firing patterns of motor units in normal rats. Nature 314:164–166

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Kern H, Pelosi L, Coletto L et al (2011) Atrophy/hypertrophy cell signaling in muscles of young athletes trained with vibrational-proprioceptive stimulation. Neurol Res 33:998–1009

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Zampieri S, Mosole S, Löfler S et al (2015) Physical exercise in Aging: nine weeks of leg press or electrical stimulation training in 70 years old sedentary elderly people. Eur J Transl Myol Basic Appl Myol 25:237–242

    Article  Google Scholar 

  23. 23.

    Kern H, Barberi L, Löfler S et al (2014) Electrical stimulation counteracts muscle decline in seniors. Front Aging Neurosci 6:189

    Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Carnio S, LoVerso F, Baraibar MA et al (2014) Autophagy impairment in muscle induces neuromuscular junction degeneration and precocious aging. Cell Rep 8:1509–1521. doi:10.1016/j.celrep.2014.07.061

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Barberi L, Scicchitano BM, Musaro A (2015) Molecular and cellular mechanisms of muscle aging and sarcopenia and effects of electrical stimulation in seniors. Eur J Transl Myol Basic Appl Myol 25:231–236

    Article  Google Scholar 

  26. 26.

    Scicchitano BM, Rizzuto E, Musarò A (2009) Counteracting muscle wasting in aging and neuromuscular diseases: the critical role of IGF-1. Aging (Albany NY) 1(5):451–457

    CAS  Article  Google Scholar 

  27. 27.

    Vinciguerra M, Musaro A, Rosenthal N (2010) Regulation of muscle atrophy in aging and disease. Adv Exp Med Biol 694:211–233

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Carosio S, Berardinelli MG, Aucello M et al (2011) Impact of ageing on muscle cell regeneration. Ageing Res Rev 10:35–42

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Barberi L, Scicchitano BM, De Rossi M et al (2013) Age-dependent alteration in muscle regeneration: the critical role of tissue niche. Biogerontology 14:273–292

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Musarò A (2014) The basis of muscle regeneration. Adv Biol 2014:1–16

    Article  Google Scholar 

  31. 31.

    Snijders T, Verdijk LB, van Loon LJ (2009) The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res Rev 8:328–338

    Article  PubMed  Google Scholar 

  32. 32.

    Mikkelsen UR, Langberg H, Helmark IC et al (2009) Local NSAID infusion inhibits satellite cell proliferation in human skeletal muscle after eccentric exercise. J Appl Physiol 107:1600–1611

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Farup J, Rahbek SK, Riis S et al (2014) Influence of exercise contraction mode and protein supplementation on human skeletal muscle satellite cell content and muscle fiber growth. J Appl Physiol 117:898–909

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Farup J, Rahbek SK, Knudsen IS et al (2014) Whey protein supplementation accelerates satellite cell proliferation during recovery from eccentric exercise. Amino Acids 46:2503–2516

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    McKay BR, Ogborn DI, Bellamy LM et al (2012) Myostatin is associated with age related human muscle stem cell dysfunction. FASEB J 26:2509–2521

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Sandri M, Barberi L, Bijlsma AY et al (2013) Signalling pathways regulating muscle mass in ageing skeletal muscle: the role of the IGF1-Akt-mTOR-FoxO pathway. Biogerontology 14:303–323

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Kadi F, Schjerling P, Andersen LL et al (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. Physiol J 558:1005–1012

    CAS  Article  Google Scholar 

  39. 39.

    Mackey AL, Holm L, Reitelseder S et al (2010) Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity. Scand J Med Sci Sports 21:773–782

    Article  PubMed  Google Scholar 

  40. 40.

    Adamo ML, Farrar RP (2006) Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev 5:310–331

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Wallace JD, Cuneo RC, Baxter R et al (1999) Responses of the growth hormone (GH) and insulin-like growth factor axis to exercise, GH administration, and GH withdrawal in trained adult males: a potential test for GH abuse in sport. J Clin Endocrinol Metab 84:3591–3601

    CAS  PubMed  Google Scholar 

  42. 42.

    Kostka T, Patricot MC, Mathian B et al (2003) Anabolic and catabolic hormonal responses to experimental two-set low-volume resistance exercise in sedentary and active elderly people. Aging Clin Exp Res 15:123–130

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Berg U, Bang P (2004) Exercise and circulating insulin-like growth factor I. Horm Res 62:50–58

    CAS  PubMed  Google Scholar 

  44. 44.

    Pelosi L, Berardinelli MG, De Pasquale L (2015) Functional and morphological improvement of dystrophic muscle by interleukin 6 receptor blockade. EBioMedicine 2:274–275

    Article  Google Scholar 

  45. 45.

    Nieto-Estévez V, Defterali Ç, Vicario-Abejón C (2016) IGF-I: a key growth factor that regulates neurogenesis and synaptogenesis from embryonic to adult stages of the brain. Front Neurosci 10:52. doi:10.3389/fnins.2016.00052

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Apel PJ, Ma J, Callahan M et al (2010) Effect of locally delivered IGF-1 on nerve regeneration during aging: an experimental study in rats. Muscle Nerve 41:335–341. doi:10.1002/mus.21485

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Wang J, Jokerst JV (2016) Stem cell imaging: tools to improve cell delivery and viability. Stem Cells Int 2016:9240652. doi:10.1155/2016/9240652

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Tezuka T, Inoue A, Hoshi T et al (2014) The MuSK activator agrin has a separate role essential for postnatal maintenance of neuromuscular synapses. Proc Natl Acad Sci USA 111:16556–16561. doi:10.1073/pnas.1408409111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Krenn M, Haller M, Bijak M et al (2011) Safe neuromuscular electrical stimulator designed for the elderly. Artif Organs 35:253–256

    Article  PubMed  Google Scholar 

  50. 50.

    He Y, Huang C, Lin X et al (2013) MicroRNA-29 family, a crucial therapeutic target for fibrosis diseases. Biochimie 95:1355–1359

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Carraro U, Franceschi C (1997) Apoptosis of skeletal and cardiac muscles and physical exercise. Aging 9(1–2):19–34 (Review)

    CAS  PubMed  Google Scholar 

  52. 52.

    Hamar D (2015) Universal linear motor driven Leg Press Dynamometer and concept of Serial Stretch Loading. Eur J Transl Myol Basic Appl Myol 25:215–219

    Article  Google Scholar 

  53. 53.

    Cvecka J, Tirpakova V, Sedliak M et al (2015) Physical activity in elderly. Eur J Transl Myol Basic Appl Myol 25:249–252

    Article  Google Scholar 

  54. 54.

    Sarabon N, Löfler S, Hosszu G et al (2015) Mobility test protocols for the elderly: a methodological note. Eur J Transl Myol Basic Appl Myol 25:253–256

    Article  Google Scholar 

  55. 55.

    Kern H (1995) Funktionelle Elektrostimulation Paraplegischer Patienten. Österreichi sche Zeitschrift für Physikalische Medizin: ÖZPM 5:1–75. ISSN 1021-4348

  56. 56.

    Kern H, Boncompagni S, Rossini K et al (2004) Long-term denervation in humans causes degeneration of both contractile and excitation contraction coupling apparatus, which is reversible by functional electrical stimulation (FES). A role for myofiber regeneration? J Neuropathol Exp Neurol 63:919–931

    Article  PubMed  Google Scholar 

  57. 57.

    Kern H, Rossini K, Carraro U et al (2005) Muscle biopsies show that FES of denervated muscles reverses human muscle degeneration from permanent spinal motoneuron lesion. J Rehabil Res Dev 42:43–53

    Article  PubMed  Google Scholar 

  58. 58.

    Boncompagni S, Kern H, Rossini K et al (2007) Structural differentiation of skeletal muscle fibers in the absence of innervation in humans. Proc Natl Acad Sci USA 104:19339–19344

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Kern H, Hofer C, Mayr W (2008) Protocols for clinical work package of the European project RISE. Eur J Transl Myol Basic Appl Myol 18:39–44

    Google Scholar 

  60. 60.

    Kern H, Carraro U, Adami N et al (2010) One year of home-based Functional Electrical Stimulation (FES) in complete lower motor neuron paraplegia: recovery of tetanic contractility drives the structural improvements of denervated muscle. Neurol Res 32:5–12. doi:10.1189/184313209X385644

    Article  PubMed  Google Scholar 

  61. 61.

    Kern H, Carraro U, Adami N et al (2010) Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair 24:709–721. doi:10.1177/1545968310366129

    Article  PubMed  Google Scholar 

  62. 62.

    Rossini K, Zanin ME, Carraro U (2002) To stage and quantify regenerative myogenesis in human long-term permanent denervated muscle. Basic Appl Myol 12:277–287

    Google Scholar 

  63. 63.

    Carraro U, Rossini K, Mayr W et al (2005) Muscle fiber regeneration in human permanent lower motoneuron denervation: relevance to safety and effectiveness of FES-training, which induces muscle recovery in SCI subjects. Artif Organs 29:187–191

    Article  PubMed  Google Scholar 

  64. 64.

    Kern H, Hofer C, Mödlin M et al (2008) Stable muscle atrophy in long-term paraplegics with complete upper motor neuron lesion from 3- to 20-year SCI. Spinal Cord 46:293–304

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Kern H, Carraro U (2014) Home-based Functional Electrical Stimulation (h-b FES) for long-term denervated human muscle: history, basics, results and perspectives of the Vienna Rehabilitation Strategy. Eur J Transl Myol Basic Appl Myol 24:27–40

    Google Scholar 

  66. 66.

    Gargiulo P, Helgason T, Reynisson PJ et al (2011) Monitoring of muscle and bone recovery in spinal cord injury patients treated with electrical stimulation using three-dimensional imaging and segmentation techniques: methodological assessment. Artif Organs 35:275–281. doi:10.1111/j.1525-1594.2011.01214.x

    Article  PubMed  Google Scholar 

  67. 67.

    Gargiulo P, Reynisson PJ, Helgason B et al (2011) Muscle, tendons, and bone: structural changes during denervation and FES treatment. Neurol Res 33:750–758. doi:10.1179/1743132811Y.0000000007

    Article  PubMed  Google Scholar 

  68. 68.

    Carraro U, Edmunds KJ, Gargiulo P (2015) 3D false color computed tomography for diagnosis and follow-up of permanent denervated human muscles submitted to home-based Functional Electrical Stimulation. Eur J Transl Myol Basic Appl Myol 25:129–140

    Article  Google Scholar 

  69. 69.

    Eberstein A, Eberstein S (1996) Electrical stimulation of denervated muscle: is it worthwhile? Med Sci Sports Exerc 28:1463–1469

    CAS  Article  PubMed  Google Scholar 

  70. 70.

    Salmons S, Ashley Z, Sutherland H et al (2005) Functional electrical stimulation of denervated muscles: basic issues. Artif Organs 29:199–202

    Article  PubMed  Google Scholar 

  71. 71.

    Carraro U, Boncompagni S, Gobbo V et al (2015) Persistent muscle fiber regeneration in long term denervation. Past, present, future. Eur J Transl Myol Basic Appl Myol 25:77–92

    Article  Google Scholar 

  72. 72.

    Brown MC, Holland RL (1979) A central role for denervated tissues in causing nerve sprouting. Nature 282(5740):724–726

    CAS  Article  PubMed  Google Scholar 

  73. 73.

    Nishimune H, Stanford JA, Mori Y (2014) Role of exercise in maintaining the integrity of the neuromuscular junction. Muscle Nerve 49:315–324. doi:10.1002/mus.24095

    CAS  Article  PubMed  Google Scholar 

  74. 74.

    Eberstein A, Pachter BR (1986) The effect of electrical stimulation on reinnervation of rat muscle: contractile properties and endplate morphometry. Brain Res 384:304–310

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Willand MP, Chiang CD, Zhang JJ et al (2015) Daily electrical muscle stimulation enhances functional recovery following nerve transection and repair in rats. Neurorehabil Neural Repair 29:690–700. doi:10.1177/1545968314562117

    Article  PubMed  Google Scholar 

  76. 76.

    Willand MP, Nguyen MA, Borschel GH et al (2015) Electrical stimulation to promote peripheral nerve regeneration. Neurorehabil Neural Repair (Epub ahead of print) (Review)

  77. 77.

    Willand MP, Nguyen MA, Borschel GH, Gordon T (2016) Electrical stimulation to promote peripheral nerve regeneration. Neurorehabil Neural Repair 30(5):490–496. doi:10.1177/1545968315604399

    Article  PubMed  Google Scholar 

  78. 78.

    Chan KM, Curran M, Gordon T (2016) The use of brief post-surgical low frequency electrical stimulation to enhance nerve regeneration in clinical practice. J Physiol. doi:10.1113/JP270892

    Google Scholar 

  79. 79.

    Wang R, Meinel FG, Schoepf UJ et al (2015) Performance of automated software in the assessment of segmental left ventricular function in cardiac CT: comparison with cardiac magnetic resonance. Eur Radiol (Epub ahead of print)

  80. 80.

    Bersch I, Tesini S, Bersch U et al (2015) Functional electrical stimulation in spinal cord injury: clinical evidence versus daily practice. Artif Organs 39:849–854. doi:10.1111/aor.12618

    Article  PubMed  Google Scholar 

  81. 81.

    Donovan-Hall MK, Burridge J, Dibb B et al (2011) The views of people with spinal cord injury about the use of functional electrical stimulation. Artif Organs 35:204–211. doi:10.1111/j.1525-1594.2011.01211.x

    Article  PubMed  Google Scholar 

  82. 82.

    Hughes AM, Burridge JH, Demain SH et al (2014) Translation of evidence-based assistive technologies into stroke rehabilitation: users’ perceptions of the barriers and opportunities. BMC Health Serv Res 14:124. doi:10.1186/1472-6963-14-124

    Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Schils SJ, Turner TA (2014) Functional Electrical Stimulation for equine epaxial muscle spasms: retrospective study of 241 clinical cases. Comp Exerc Physiol 10:89–97

    Article  Google Scholar 

  84. 84.

    Ravara B, Gobbo V, Carraro U et al (2015) Functional electrical stimulation as a safe and effective treatment for equine epaxial muscle spasms: clinical evaluations and histochemical morphometry of mitochondria in muscle biopsies. Eur J Transl Myol Basic Appl Myol 25:109–120

    Article  Google Scholar 

  85. 85.

    Schils S, Carraro U, Turner T et al (2015) Functional electrical stimulation for equine muscle hypertonicity: histological changes in mitochondrial density and distribution. J Equine Vet Sci 35:907–916

    Article  Google Scholar 

  86. 86.

    Mosole S, Zampieri S, Germinario E et al (2015) Structural and functional characteristics of denervated muscles from oldest-old rats: a relevant animal model for FES of denervated myofibers of the diaphragm in ALS? Eur J Transl Myol Basic Appl Myol 25:151

    Google Scholar 

  87. 87.

    Mammucari C, Gherardi G, Zamparo I et al (2015) The mitochondrial calcium uniporter controls skeletal muscle trophism in vivo. Cell Rep 2015(10):1269–1279. doi:10.1016/j.celrep.01.056

    Article  Google Scholar 

  88. 88.

    Franzini-Armstrong C (2015) Electron microscopy: from 2D to 3D images with special reference to muscle. Eur J Transl Myol Basic Appl Myol 25(1):5–13

    Article  Google Scholar 

  89. 89.

    Cheetham J, Perkins JD, Jarvis JC et al (2015) Effects of functional electrical stimulation on denervated laryngeal muscle in a large animal model. Artif Organs 39(10):876–885. doi:10.1111/aor.12624

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the European Regional Development Fund—Cross Border Cooperation Programme Slovakia—Austria 2007–2013 (Interreg-IVa), project Mobilität im Alter, MOBIL, N_00033 (Partners: Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Austria, Center for Medical Physics and Biomedical Engineering, Medical University of Vienna, Austria, and Faculty of Physical Education and Sports, Comenius University in Bratislava, Slovakia); Austrian national co-financing of the Austrian Federal Ministry of Science and Research; Ludwig Boltzmann Society (Vienna, Austria) and supported by EU Commission Shared Cost Project RISE (Contract No. QLG5-CT-2001-02191) co-financed by the Austrian Ministry of Science. Some of the research reported in this publication was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the National Institutes of Health under Award Number NIH NIAMS 1R03AR053706-01A2 to ALP. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Ugo Carraro thanks the IRCCS Fondazione Ospedale San Camillo, Venice, Italy for hospitality and scientific support.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Simone Mosole.

Ethics declarations

Conflict of interest

None.

Ethical approval

All participants in the senior sportsmen studies were healthy and declared not to have any specific physical/disease issues (for detailed inclusion and exclusion criteria, see ClinicalTrials.gov: NCT01679977). All of the senior sportsmen declared to have a lifelong (30 years) history of high-level training. We certify that all applicable rules concerning the ethical use of human volunteers were followed during the course of this research (approval of ethical committee, Vienna, Austria: EK-02-068-0702).

Human and Animal Rights

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual partecipants included in the study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carraro, U., Kern, H., Gava, P. et al. Recovery from muscle weakness by exercise and FES: lessons from Masters, active or sedentary seniors and SCI patients. Aging Clin Exp Res 29, 579–590 (2017). https://doi.org/10.1007/s40520-016-0619-1

Download citation

Keywords

  • Aging
  • Master Athletes
  • Muscle
  • Denervation and type grouping
  • FES recovery
  • Muscle Color Computed Tomography