https://doi.org/10.4081/ejtm.2022.10420

Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise (2013, revisited here in 2022)

Vol. 32 No. 1 (2022)
Published: 28 February 2022
Aging, human skeletal muscle, lifelong physical exercise, senior sportsmen, denervation and reinnervation, fiber-type grouping; training
Abstract Views: 1038
PDF: 504
HTML: 23
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Simone Mosole
Laboratory of Translation Myology, Department of Biomedical Sciences, Padua, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Katia Rossini
Laboratory of Translation Myology, Department of Biomedical Sciences, Padua, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Helmut Kern
Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Stefan Löfler
Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Hannah Fruhmann
Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Michael Vogelauer
Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna, Austria.
Samantha Burggraf
Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Austria.
Martina Grim-Stieger
Department of Physical Medicine and Rehabilitation, Wilhelminenspital, Vienna, Austria.
Ján Cvečka
Faculty of Physical Education and Sport, Comenius University, Bratislava, Slovakia.
Dušan Hamar
Faculty of Physical Education and Sport, Comenius University, Bratislava, Slovakia.
Milan Sedliak
Faculty of Physical Education and Sport, Comenius University, Bratislava, Slovakia.
Nejc Šarabon
University of Primorska, Science and Research Centre, Institute for Kinesilogical Research, Koper, Slovenia.
Amber Pond
Anatomy Department, Southern Illinois University School of Medicine, Carbondale, IL, United States.
Donatella Biral
C.N.R. Institute of Neuroscience, Department of Biomedical Sciences, Padua, Italy.
Ugo Carraro
http://orcid.org/0000-0002-0924-4998
Laboratory of Translation Myology, Department of Biomedical Sciences, Padua, Italy.
Sandra Zampieri
sanzamp@unipd.it
Laboratory of Translation Myology, Department of Biomedical Sciences, Padua, Italy; Ludwig Boltzmann Institute of Electrical Stimulation and Physical Rehabilitation, Vienna, Italy.

In 2013 we presented results showing that at the histological level lifelong increased physical activity promotes reinnervation of muscle fibers in aging muscles. Indeed, in muscle biopsies from 70-year old men with a lifelong history of high-level physical activity, we observed a considerable increase in fiber-type groupings (F-TG), almost exclusively of the slow type. Slow-type transformation by denervation-reinnervation in senior sportsmen seems to fluctuate from those with scarce fiber-type transformation and groupings to almost fully transformed muscle, going through a process in which isolated fibers co-expressing fast and slow Myosin Heavy Chains (MHCs) seems to fill the gaps. Taken together, our results suggest that, beyond the direct effects of aging on the muscle fibers, changes occurring in skeletal muscle tissue appear to be largely, although not solely, a result of sparse denervation-reinnervation. The lifelong exercise allows the body to adapt to the consequences of the age-related denervation and to preserve muscle structure and function by saving otherwise lost muscle fibers through recruitment to different, mainly slow, motor units. These beneficial effects of high-level life-long exercise on motoneurons, specifically on the slow type motoneurones that are those with higher daily activity, and on muscle fibers, serve to maintain size, structure and function of muscles, delaying the functional decline and loss of independence that are commonly seen in late aging. Several studies of independent reserchers with independent analyses confirmed and cited our 2013 results. Thus, the results we presented in our paper in 2013 seem to have held up rather well.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Crossref
Scopus
Google Scholar
Europe PMC
Tomlinson BE, Walton JN, Rebeiz JJ. The effects of ageing and of cachexia upon skeletal muscle. A histopathological study. J Neurol Sci 1969;9:321-346. DOI: https://doi.org/10.1016/0022-510X(69)90079-3
Urbanchek MG, Picken EB, Kalliainen LK, Kuzon WM Jr. Specific force deficit in skeletal muscles of old rats is partially explained by the existence of denervated muscle fibers. J Gerontol A Biol Sci Med Sci 2001;56:B191–B197. DOI: https://doi.org/10.1093/gerona/56.5.B191
Tomlinson BE, Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 1977;34:213-219. DOI: https://doi.org/10.1016/0022-510X(77)90069-7
Doherty TJ, Vandervoort AA, Taylor AW, Brown WF. Effects of motor unit losses on strength in older men and women. J Appl Physiol 1993;74: 868-874. DOI: https://doi.org/10.1152/jappl.1993.74.2.868
Andersen JL. Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 2003;13:40–47. DOI: https://doi.org/10.1034/j.1600-0838.2003.00299.x
Luff AR. Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann N Y Acad Sci 1998;854:92-101. DOI: https://doi.org/10.1111/j.1749-6632.1998.tb09895.x
Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 2012;3:260. DOI: https://doi.org/10.3389/fphys.2012.00260
Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev 2011;91:1447-1531. DOI: https://doi.org/10.1152/physrev.00031.2010
D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol (Lond.) 2003;552:499–511. DOI: https://doi.org/10.1113/jphysiol.2003.046276
Carraro U. Modulation of trophism and fiber type expression of denervated muscle by different patterns of electrical stimulation. Basic Appl Myol 2002;12:263-273.
Carraro U, Catani C, Belluco S, Cantini M, Marchioro L. Slow-like electrostimulation switches on slow myosin in denervated fast muscle. Exp Neurol 1986;94:537-553. DOI: https://doi.org/10.1016/0014-4886(86)90236-0
Kern H, Carraro U, Adami N, Biral D, Hofer C, Forstner C, Mödlin M, Vogelauer M, Pond A, Boncompagni S, Paolini C, Mayr W, Protasi F, Zampieri S. Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair 2010;24:709-721. DOI: https://doi.org/10.1177/1545968310366129
Mayne CN, Mokrusch T, Jarvis JC, Gilroy SJ, Salmons S. Stimulation-induced expression of slow muscle myosin in a fast muscle of the rat. Evidence of an unrestricted adaptive capacity. FEBS Lett 1993;327:297-300. DOI: https://doi.org/10.1016/0014-5793(93)81008-N
Midrio M. The denervated muscle: facts and hypotheses. A historical review. Eur J Appl Physiol 2006;98:1-21. Epub 2006 Aug 3. DOI: https://doi.org/10.1007/s00421-006-0256-z
Salmons S. Exercise, stimulation and type transformation of skeletal muscle. Int J Sports Med 1994;15:136-141. Review. DOI: https://doi.org/10.1055/s-2007-1021035
Coggan AR, Spina RJ, Rogers MA, King DS, Brown M, Nemeth PM, Holloszy JO. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol 1990;68:1896-1901. DOI: https://doi.org/10.1152/jappl.1990.68.5.1896
Trappe S. Master athletes. Int J Sport Nutr Exerc Metab 2001;11Suppl:S196-207. DOI: https://doi.org/10.1123/ijsnem.11.s1.s196
Wright VJ, Perricelli BC. Age-related rates of decline in performance among elite senior athletes. Am J Sports Med 2008;36:443-450. Epub 2007 Nov 30. DOI: https://doi.org/10.1177/0363546507309673
Kern H, Loefler S, Burggraf S, Fruhmann H, Cvecka J, Sedliak M, Barberi L, De Rossi M, Musarò A, Carraro U, Mosole S, Zampieri S. Electrical stimulation counteracts muscle atrophy associated with aging in humans. European Journal Translational Myology - Basic Applied Myology 2013;23:105-108. DOI: https://doi.org/10.4081/bam.2013.3.105
Zampieri S, Rossini K, Carraro U, Kern H. Morphometry of skeletal muscle in sedentary elderly and senior sportsmen. European Journal Translational Myology - Basic Applied Myology 2012;22:13.
Rossini K, Zanin ME, Podhorska-Okolow M, Carraro U. To stage and quantify regenerative myogenesis in human long-term permanent denervated muscle. Basic Appl Myol 2002;12:277-286.
Kern H, Boncompagni S, Rossini K, Mayr W, Fanò G, Zanin ME, Podhorska-Okolow M, Protasi F, Carraro U. Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus that can be reversed by functional electrical stimulation (FES). A role for myofiberegeneration? J Neuropath Exp Neurol 2004;63:919-931. DOI: https://doi.org/10.1093/jnen/63.9.919
Kern H, Carraro U, Adami N, Hofer C, Loefler S, Vogelauer M, Mayr W, Rupp R, Zampieri S. One year of home-based daily FES in complete lower motor neuron paraplegia: recovery of tetanic contractility drives the structural improvements of denervated muscle. Neurol Res 2010;32:5-12. DOI: https://doi.org/10.1179/174313209X385644
Kern H, Hofer C, Mödlin M, Mayr W, Vindigni V, Zampieri S, Boncompagni S, Protasi F, Carraro U. Stable muscle atrophy in long-term paraplegics with complete upper motor neuron lesion from 3- to 20-year SCI. Spinal Cord 2008;46:293-304. DOI: https://doi.org/10.1038/sj.sc.3102131
Boncompagni S, Kern H, Rossini K, Hofer C, Mayr W, Carraro U, Protasi F. Structural differentiation of skeletal muscle fibers in the absence of innervation in humans. Proc Natl Acad Sci USA 2007;104:19339-19344. Epub 2007 Nov 27. DOI: https://doi.org/10.1073/pnas.0709061104
Gutmann E, Hanzlikova V. Motor unit in old age. Nature 1966;209:921-922. DOI: https://doi.org/10.1038/209921b0
Scelsi R, Marchetti C, Poggi P. Histochemical and ultrastructural aspects of m. vastus lateralis in sedentary old people (aged 65-89 years). Acta Neuropathol 1980;51:99-105. DOI: https://doi.org/10.1007/BF00690450
Leyk D, Rüther T, Wunderlich M, Sievert A, Essfeld D, Witzki A, Erley O, Küchmeister G, Piekarski C, Löllgen H. Physical performance in middle age and old age: good news for our sedentary and aging society. Dtsch Arztebl Int 2010;107:809-816. DOI: https://doi.org/10.3238/arztebl.2010.0809
McNeil CJ, Doherty TJ, Stashuk DW, Rice CL. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 2005;31:461–467. DOI: https://doi.org/10.1002/mus.20276
Meltzer DE. Age dependence of olympic weightlifting ability. Med Sci Sports Exerc 1994;26:1053-1067. DOI: https://doi.org/10.1249/00005768-199408000-00019
Wroblewski AP, Amati F, Smiley MA, Goodpaster B, Wright V. Chronic exercise preserves lean muscle mass in masters athletes. Phys Sportsmed 2011;39:172-178. DOI: https://doi.org/10.3810/psm.2011.09.1933
Larsson L. Motor units: remodeling in aged animals. J Gerontol A Biol Sci Med Sci 1995:50:91-95. DOI: https://doi.org/10.1093/gerona/50A.Special_Issue.91
Lexell J, Downham DY. The occurrence of fiber- 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 (Berl) 1991;81:377-381. DOI: https://doi.org/10.1007/BF00293457
Mosole S, Carraro U, Kern H, Loefler S, Fruhmann H, Vogelauer M, Burggraf S, Mayr W, Krenn M, Paternostro-Sluga T, Hamar D, Cvecka J, Sedliak M, Tirpakova V, Sarabon N, Musarò A, Sandri M, Protasi F, Nori A, Pond A, Zampieri S. Long-term high-level exercise promotes muscle reinnervation with age. J Neuropathol Exp Neurol. 2014 Apr;73(4):284-94. DOI: https://doi.org/10.1097/NEN.0000000000000032
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: https://doi.org/10.3389/fnagi.2014.00189
Mosole S, Rossini K, Kern H, Löfler S, Simone Fruhmann H, Vogelauer M, Burggraf S, Grim-Stieger M, Cvečka J, Hamar D, Sedliak M, Šarabon N, Pond A, Biral D, Carraro U, Zampieri S. Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise. Eur J Transl Myol Basic Appl Myol. 2013;23 (4):205–210. DOI: https://doi.org/10.4081/bam.2013.4.205
Ugo Carraro, Laboratory of Translation Myology, Department of Biomedical Sciences, Padua

CURRICULUM VITAE: Prof. UGO CARRARO

ORCID iD: http://orcid.org/0000-0002-0924-4998

Prof. Ugo Carraro, M.D.,

Senior Scholar of the University of Padova, Italy

Department of Biomedical Sciences, University of Padova, Italy

phone: +39 338 1575745

E-mail: ugo.carraro@unipd.it

 

Born:                      February 23, 1943, Abano Terme (Padova), Italy

Citizenship:           Italy

Degree and Academic Positions

-       M.D. (Laurea in Medicina e Chirurgia), University of Padua, Italy -1968

-       Associate Professor of General Pathology, Faculty of Medicine, University of Padova,1983-2013

-       Principal Investigator of the Laboratory of Applied Myology of the C.N.R Institute of Neuroscience, 1983-2000

-       Acting-director of the Department of Biomedical Science -1998 to 2003;

-       Principal Investigator of the Translational Myology Lab, Department of Biomedical Science -1998 to 2013

-       Interdepartmental Research Center of Myology (cirMYO), Founder and Head 2005 - 2011

Other Professional Activities

-       1991-2019 – Founder and Editor-in-Chief of Basic Applied Myology: 1991 to date

-       Consultant of I.R.C.C.S. Ospedale San Camillo di Venezia-Lido, Italy

-        Referee for International Journals and Granting Agencies: J Cell Biol, Muscle&Nerve, Artificial Organs, J Muscle Res Cell Motility, Artificial Organs, Cell Death & Differentiation, Annals Thoracic Surgery, Acta Physiologica, The Open Rehabilitation Journal, Association Française contre les Myopathies

-       Organizer of International Conferences and Courses

-       Invited speaker and chairman in International Conferences

Main Research Interests

-       Translational Myology: Basics of muscle plasticity and their applications to medical research, in particular:

  • Functional Electrical Stimulation (FES) of denervated human muscle
  • Role of regenerative myogenesis in exercise-induced muscle damage and denervation
  • Reconstruction, neurotization and artificial synaptogenesis of ablated skeletal muscle
  • Analyses in muscle atrophy and apoptosis of role of Cytokines and Myokines by invasive and non-invasive samplings

 

Achievments and expertises

Prof. Ugo Carraro is a world-class leader in molecular and structural analyses of skeletal muscle. He developed bi-dimensional gel electrophoresis for myosin light chains, in particular the embryonic isoform, and was the first to separate human myosin heavy chain isoforms.

He discovered the long-term potential of denervated muscle to survive denervation by non-compensatory myofiber regeneration.

Prof. Carraro was Associate Professor of General Pathology at the Faculty of Medicine of the University of Padova, from 1983 to 2013. Editor-in-Chief of The European Journal of Translational Myology since 1991, he founded and chaired from 2005 to 2011 Interdepartmental Research Center of Myology (CIR-Myo) of the University of Padova. CIR-Myo continue to join scientists and clinicians of the Departments of Biology, Biomedical Sciences, Neuroscience, Medicine and Surgical Sciences, Physical Medicine and Rehabilitation and Experimental & Clinical Veterinary Sciences.

In collaboration with international partners, in particular the Ludwig Boltzmann Institute of Electrostimulation and Physical Rehabilitation of the Wilheminenspital, Vienna, Austria, CIR-Myo scientists and clinicians developed and implemented the expertise and facilities to maintain and extend in Interreg IVa a world-unique BIO-BANK of human skeletal muscle biopsies harvested from upper motor neuron and lower motor neuron denervated patients and related animal research, young and senior sportsmen, healthy and diseased elderly persons before and during recovery by new therapies and rehabilitation strategies. In particular, muscle biopsies were harvested from patients affected with spinal cord injury and severe leg trauma, osteoarthropathies and rheumatic autoimmune diseases, and cancer.

CIR-Myo is developing also new imaging methods for functional monitoring of human skeletal muscles from patients suffering with permanent and transient muscle denervation. The collaboration with the Dr. Kern’s Vienna Group resulted in new knowledge and clinical validation of rehabilitation strategies for permanently denervated human muscles using home-based Functional Electrical Stimulation (FES). Thus, a world unique human muscle biopsies DATA-BASE of structural and molecular data obtained by histology, histo- and immuno-chemistry, electron microscopy and genomic/proteomic approaches is available to compare new rehabilitation strategies against standard clinical methods.

Carraro’s Lab matured expertises working on different aspects of muscle biology and pathology, including spinal cord injuries, aging, apoptosis, and muscle regeneration. This full set of methods and expertise are uniquely present at the CIR-Myo of Padova University, and well documented by a list of original results published in leading Journals of the different research fields.

Now Professor Carraro is validating NON-INVASIVE BLOOD ANALYSES to monitor Cytokines (anti- and pro- Inflammatory) and Myokines by saliva and sweat samplings, a very promising approach that will increase acceptability of sampling by volunteering persons and frequency of sampling, a key factor to evaluate the many very transient effects of trainings and rehabilitations in early aging and aging.

Publications

PUBMED April 12, 2020: Ugo Carraro 1973 - 2019 - References: 156 - Citations > 3000 –

h-index 44;  h-index 37, excluding self-citations

List of 10 recent publications 2020-2016

  1. Ricciardi C, Edmunds KJ, Recenti M, Sigurdsson S, Gudnason V, Carraro U, Gargiulo P. Assessing cardiovascular risks from a mid-thigh CT image: a tree-based machine learning approach using radiodensitometric distributions. Sci Rep. 2020 Feb 18;10(1):2863. doi: 10.1038/s41598-020-59873-9. PMID: 32071412
  2. Carraro U. 2020PMD, 30-years of Translational Mobility Medicine at the time of COVID-19 outbreak: Last-minute forewords from the editor. Eur J Transl Myol 2020;30:8966. Doi 10.4081/ejtm.2019.8966.
  3. Albertin G, Ravara B, Kern H, Hofer C, Loefler S, Jurecka W, Guidolin D, Rambaldo A, Porzionato A, De Caro R, Zampieri S, Pond A, Alaibac M, Carraro U. Two-years of home based functional electrical stimulation recovers epidermis from atrophy and flattening after years of complete Conus-Cauda Syndrome. Medicine (Baltimore). 2019 Dec;98(52):e18509. doi: 10.1097/MD.0000000000018509. PMID: 31876739.
  4. Kern H, Gargiulo P, Pond A, Albertin G, Marcante A, Carraro U. To Reverse Atrophy of Human Muscles in Complete SCI Lower Motor Neuron Denervation by Home-Based Functional Electrical Stimulation. Adv Exp Med Biol. 2018;1088:585-591. doi: 10.1007/978-981-13-1435-3_27.
  5. Carraro U, Gava K, Baba A, Marcante A, Piccione F. To Contrast and Reverse Skeletal Muscle Atrophy by Full-Body In-Bed Gym, a Mandatory Lifestyle for Older Olds and Borderline Mobility-Impaired Persons. Adv Exp Med Biol. 2018;1088:549-560. doi: 10.1007/978-981-13-1435-3_25. Review.
  6. Carraro U. Exciting perspectives for Translational Myology in the Abstracts of the 2018Spring PaduaMuscleDays: Giovanni Salviati Memorial - Chapter I - Foreword. Eur J Transl Myol. 2018 Feb 20;28(1):7363. doi: 10.4081/ejtm.2018.7363. eCollection 2018 Jan 12.
  7. Mosole S, Zampieri S, Furlan S, Carraro U, Löefler S, Kern H, Volpe P, Nori A. Effects of Electrical Stimulation on Skeletal Muscle of Old Sedentary People. Gerontol Geriatr Med. 2018 Apr 10;4:2333721418768998. doi: 10.1177/2333721418768998. eCollection 2018 Jan-Dec.
  8. Edmunds K, Gíslason M, Sigurðsson S, Guðnason V, Harris T, Carraro U, Gargiulo P. Advanced quantitative methods in correlating sarcopenic muscle degeneration with lower extremity function biometrics and comorbidities. PLoS One. 2018 Mar 7;13(3):e0193241. doi: 10.1371/journal.pone.0193241. eCollection 2018.
  9. Atrophy, ultra-structural disorders, severe atrophy and degeneration of denervated human muscle in SCI and Kern H, Hofer C, Loefler S, Zampieri S, Gargiulo P, Baba A, Marcante A, Piccione F, Pond A, Carraro U. Aging. Implications for their recovery by Functional Electrical Stimulation, updated 2017. Neurol Res. 2017 Jul;39(7):660-666. doi: 10.1080/01616412.2017.1314906. Epub 2017 Apr 13. Review.
  10. Edmunds KJ, Árnadóttir Í, Gíslason MK, Carraro U, Gargiulo P. Nonlinear Trimodal Regression Analysis of Radiodensitometric Distributions to Quantify Sarcopenic and Sequelae Muscle Degeneration. Comput Math Methods Med. 2016;2016:8932950. doi: 10.1155/2016/8932950. Epub 2016 Dec 27.

 

How to Cite

Mosole, S., Rossini, K., Kern, H., Löfler, S., Fruhmann, H., Vogelauer, M., Burggraf, S., Grim-Stieger, M. ., Cvečka, J., Hamar, D., Sedliak, M., Šarabon, N., Pond, A., Biral, D., Carraro, U., & Zampieri, S. (2022). Reinnervation of Vastus lateralis is increased significantly in seniors (70-years old) with a lifelong history of high-level exercise (2013, revisited here in 2022). European Journal of Translational Myology, 32(1). https://doi.org/10.4081/ejtm.2022.10420

PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.


Similar Articles

You may also start an advanced similarity search for this article.