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Clark NC. Sensorimotor control of functional joint stability: Scientific concepts, clinical considerations, and the articuloneuromuscular cascade paradigm in peripheral joint injury. Musculoskelet Sci Pract 2024; 74:103198. [PMID: 39362022 DOI: 10.1016/j.msksp.2024.103198] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/24/2024] [Revised: 09/22/2024] [Accepted: 09/28/2024] [Indexed: 10/05/2024]
Abstract
Human movement depends on sensorimotor control. Sensorimotor control refers to central nervous system (CNS) control of joint stability, posture, and movement, all of which are effected via the sensorimotor system. Given the nervous, muscular, and skeletal systems function as an integrated "neuromusculoskeletal system" for the purpose of executing movement, musculoskeletal conditions can result in a cascade of impairments that affect negatively all three systems. The purpose of this article is to revisit concepts in joint stability, sensorimotor control of functional joint stability (FJS), joint instability, and sensorimotor impairments contributing to functional joint instability. This article differs from historical work because it updates previous models of joint injury and joint instability by incorporating more recent research on CNS factors, skeletal muscle factors, and tendon factors. The new 'articuloneuromuscular cascade paradigm' presented here offers a framework for facilitating further investigation into physiological and biomechanical consequences of joint injury and, in turn, how these follow on to affect physical activity (functional) capability. Here, the term 'injury' represents traumatic joint injury with a focus is on peripheral joint injury. Understanding the configuration of the sensorimotor system and the cascade of post-injury sensorimotor impairments is particularly important for clinicians reasoning rational interventions for patients with mechanical instability and functional instability. Concurrently, neurocognitive processing and neurocognitive performance are also addressed relative to feedforward neuromuscular control of FJS. This article offers itself as an educational resource and scientific asset to contribute to the ongoing research and applied practice journey for developing optimal peripheral joint injury rehabilitation strategies.
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Affiliation(s)
- Nicholas C Clark
- School of Sport, Rehabilitation, and Exercise Sciences, University of Essex, Wivenhoe Park, Colchester, Essex, CO4 3SQ, UK, United Kingdom.
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Arpke RW, Moritz TC, Hahn KL, Stark DA, Villalón E, Lorson CL, Cornelison DDW. Normal muscle fiber type distribution is recapitulated in aged ephrin-A3 -/- mice that previously lacked most slow myofibers. Am J Physiol Cell Physiol 2023; 324:C718-C727. [PMID: 36717102 PMCID: PMC10027087 DOI: 10.1152/ajpcell.00519.2022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/15/2022] [Revised: 01/18/2023] [Accepted: 01/19/2023] [Indexed: 02/01/2023]
Abstract
Individual limb muscles have characteristic representation and spatial distribution of muscle fiber types (one slow and up to three fast isoforms) appropriate to their unique anatomical location and function. This distribution can be altered by physiological stimuli such as training (i.e., for increased endurance or force) or pathological conditions such as aging. Our group previously showed that ephrin-A3 is expressed only on slow myofibers, and that adult mice lacking ephrin-A3 have dramatically reduced numbers of slow myofibers due to postnatal innervation of previously slow myofibers by fast motor neurons. In this study, fiber type composition of hindlimb muscles of aged and denervated/reinnervated C57BL/6 and ephrin-A3-/- mice was analyzed to determine whether the loss of slow myofibers persists across the lifespan. Surprisingly, fiber-type composition of ephrin-A3-/- mouse muscles at two years of age was nearly indistinguishable from age-matched C57BL/6 mice. After challenge with nerve crush, the percentage of IIa and I/IIa hybrid myofibers increased significantly in aged ephrin-A3-/- mice. While EphA8, the receptor for ephrin-A3, is present at all neuromuscular junctions (NMJs) on fast fibers in 3-6 mo old C57BL/6 and ephrin-A3-/- mice, this exclusive localization is lost with aging, with EphA8 expression now found on a subset of NMJs on some slow muscle fibers. This return to appropriate fiber-type distribution given time and under use reinforces the role of activity in determining fiber-type representation and suggests that, rather than being a passive baseline, the developmentally and evolutionarily selected fiber type pattern may instead be actively reinforced by daily living.
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Affiliation(s)
- Robert W. Arpke
- Division of Biological Sciences, University of Missouri, Columbia, Missouri, United States
- Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, United States
| | - Timothy C. Moritz
- Division of Biological Sciences, University of Missouri, Columbia, Missouri, United States
| | - Kevin L. Hahn
- Division of Biological Sciences, University of Missouri, Columbia, Missouri, United States
| | - Danny A. Stark
- Division of Biological Sciences, University of Missouri, Columbia, Missouri, United States
- Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, United States
| | - Eric Villalón
- Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, United States
| | - Christian L. Lorson
- Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, United States
| | - DDW Cornelison
- Division of Biological Sciences, University of Missouri, Columbia, Missouri, United States
- Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, United States
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Gouveia D, Cardoso A, Carvalho C, Almeida A, Gamboa Ó, Ferreira A, Martins Â. Approach to Small Animal Neurorehabilitation by Locomotor Training: An Update. Animals (Basel) 2022; 12:ani12243582. [PMID: 36552502 PMCID: PMC9774773 DOI: 10.3390/ani12243582] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/20/2022] [Revised: 12/05/2022] [Accepted: 12/15/2022] [Indexed: 12/23/2022] Open
Abstract
Neurorehabilitation has a wide range of therapies to achieve neural regeneration, reorganization, and repair (e.g., axon regeneration, remyelination, and restoration of spinal circuits and networks) to achieve ambulation for dogs and cats, especially for grade 1 (modified Frankel scale) with signs of spinal shock or grade 0 (deep pain negative), similar to humans classified with ASIA A lesions. This review aims to explain what locomotor training is, its importance, its feasibility within a clinical setting, and some possible protocols for motor recovery, achieving ambulation with coordinated and modulated movements. In addition, it cites some of the primary key points that must be present in the daily lives of veterinarians or rehabilitation nurses. These can be the guidelines to improve this exciting exercise necessary to achieve ambulation with quality of life. However, more research is essential in the future years.
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Affiliation(s)
- Débora Gouveia
- Arrábida Veterinary Hospital—Arrábida Animal Rehabilitation Center, 2925-538 Setubal, Portugal
- Superior School of Health, Protection and Animal Welfare, Polytechnic Institute of Lusophony, Campo Grande, 1950-396 Lisboa, Portugal
- Faculty of Veterinary Medicine, Lusófona University, Campo Grande, 1749-024 Lisboa, Portugal
- Correspondence:
| | - Ana Cardoso
- Arrábida Veterinary Hospital—Arrábida Animal Rehabilitation Center, 2925-538 Setubal, Portugal
| | - Carla Carvalho
- Arrábida Veterinary Hospital—Arrábida Animal Rehabilitation Center, 2925-538 Setubal, Portugal
| | - António Almeida
- Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisboa, Portugal
| | - Óscar Gamboa
- Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisboa, Portugal
| | - António Ferreira
- Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisboa, Portugal
- CIISA—Centro Interdisciplinar-Investigaçāo em Saúde Animal, Faculdade de Medicina Veterinária, Av. Universi dade Técnica de Lisboa, 1300-477 Lisboa, Portugal
| | - Ângela Martins
- Arrábida Veterinary Hospital—Arrábida Animal Rehabilitation Center, 2925-538 Setubal, Portugal
- Superior School of Health, Protection and Animal Welfare, Polytechnic Institute of Lusophony, Campo Grande, 1950-396 Lisboa, Portugal
- Faculty of Veterinary Medicine, Lusófona University, Campo Grande, 1749-024 Lisboa, Portugal
- Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisboa, Portugal
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Furlan JC, Pakosh M, Craven BC, Popovic MR. Insights on the Potential Mechanisms of Action of Functional Electrical Stimulation Therapy in Combination With Task-Specific Training: A Scoping Review. Neuromodulation 2022; 25:1280-1288. [PMID: 34031937 DOI: 10.1111/ner.13403] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/25/2020] [Revised: 03/12/2021] [Accepted: 03/30/2021] [Indexed: 12/01/2022]
Abstract
OBJECTIVES This scoping review was undertaken to synthetize and appraise the literature on the potential mechanisms of action of functional electrical stimulation therapy in combination with task-specific training (FEST + TST) in the rehabilitation following stroke, spinal cord injury, traumatic brain injury, or multiple sclerosis. MATERIALS AND METHODS The literature search was performed using multiple databases (including APA, PsycInfo, Medline, PubMed, EMBASE, CCRCT, and Cochrane Database of Systematic Reviews) from 1946 to June 2020. The literature search used the following terms: (spinal cord injury, paraplegia, tetraplegia, quadriplegia, stroke, multiple sclerosis, traumatic brain injury, or acquired brain injury) AND (functional electrical stimulation or FES). The search included clinical and preclinical studies without limits to language. RESULTS Of the 8209 titles retrieved from the primary search, 57 publications fulfilled the inclusion and exclusion criteria for this scoping review. While most publications were clinical studies (n = 50), there were only seven preclinical studies using animal models. The results of this review suggest that FEST + TST can result in multiple effects on different elements from the muscle to the cerebral cortex. However, most studies were focused on the muscle changes after FEST + TST. CONCLUSIONS The results of this scoping review suggest that FEST + TST can result in multiple effects on different elements of the neuromuscular system, while most research studies were focused on the muscle changes after FEST + TST. Despite the efficacy of the FEST + TST in the neurorehabilitation after CNS injury or disease, the results of this review underline an important knowledge gap with regards to the actual mechanism of action of FEST + TST.
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Affiliation(s)
- Julio Cesar Furlan
- Department of Medicine, Division of Physical Medicine and Rehabilitation, University of Toronto, Toronto, ON, Canada; Lyndhurst Centre, Toronto Rehabilitation Institute, University Health Network, Toronto, ON, Canada; KITE - Research Institute, University Health Network, Toronto, ON, Canada; Institute of Medical Science, University of Toronto, Toronto, ON, Canada; Rehabilitation Sciences Institute, University of Toronto, Toronto, ON, Canada; Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, ON, Canada.
| | - Maureen Pakosh
- Library & Information Services, Rumsey Cardiac Centre Library, University Health Network, Toronto Rehabilitation Institute, Toronto, ON, Canada
| | - Beverley Catharine Craven
- Department of Medicine, Division of Physical Medicine and Rehabilitation, University of Toronto, Toronto, ON, Canada; Lyndhurst Centre, Toronto Rehabilitation Institute, University Health Network, Toronto, ON, Canada; KITE - Research Institute, University Health Network, Toronto, ON, Canada
| | - Milos Radomir Popovic
- KITE - Research Institute, University Health Network, Toronto, ON, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON, Canada
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S. Baptista R, C. C. Moreira M, D. M. Pinheiro L, R. Pereira T, G. Carmona G, P. D. Freire J, A. I. Bastos J, Padilha Lanari Bo A. User-centered design and spatially-distributed sequential electrical stimulation in cycling for individuals with paraplegia. J Neuroeng Rehabil 2022; 19:45. [PMID: 35527249 PMCID: PMC9080548 DOI: 10.1186/s12984-022-01014-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2021] [Accepted: 03/28/2022] [Indexed: 11/10/2022] Open
Abstract
Abstract
Background
In this work, we share the enhancements made in our system to take part in the CYBATHLON 2020 Global Edition Functional Electrical Stimulation (FES) Bike Race. Among the main improvements, firstly an overhaul, an overhaul of the system and user interface developed with User-centered design principles with remote access to enable telerehabilitation. Secondly, the implementation and experimental comparison between the traditional single electrode stimulation (SES) and spatially distributed sequential stimulation (SDSS) applied for FES Cycling.
Methods
We report on the main aspects of the developed system. To evaluate the user perception of the system, we applied a System Usability Scale (SUS) questionnaire. In comparing SDSS and SES, we collected data from one subject in four sessions, each simulating one race in the CYBATHLON format.
Results
User perception measured with SUS indicates a positive outcome in the developed system. The SDSS trials were superior in absolute and average values to SES regarding total distance covered and velocity. We successfully competed in the CYBATHLON 2020 Global Edition, finishing in 6th position in the FES Bike Race category.
Conclusions
The CYBATHLON format induced us to put the end-user in the center of our system design principle, which was well perceived. However, further improvements are required if the intention is to progress to a commercial product. FES Cycling performance in SDSS trials was superior when compared to SES trials, indicating that this technique may enable faster and possibly longer FES cycling sessions for individuals with paraplegia. More extensive studies are required to assess these aspects.
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Duffell LD, Donaldson NDN. A Comparison of FES and SCS for Neuroplastic Recovery After SCI: Historical Perspectives and Future Directions. Front Neurol 2020; 11:607. [PMID: 32714270 PMCID: PMC7344227 DOI: 10.3389/fneur.2020.00607] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/11/2020] [Accepted: 05/25/2020] [Indexed: 12/17/2022] Open
Abstract
There is increasing evidence that neuroplastic changes can occur even years after spinal cord injury, leading to reduced disability and better health which should reduce the cost of healthcare. In motor-incomplete spinal cord injury, recovery of leg function may occur if repetitive training causes afferent input to the lumbar spinal cord. The afferent input may be due to activity-based therapy without electrical stimulation but we present evidence that it is faster with electrical stimulation. This may be spinal cord stimulation or peripheral nerve stimulation. Recovery is faster if the stimulation is phasic and that the patient is trying to use their legs during the training. All the published studies are small, so all conclusions are provisional, but it appears that patients with more disability (AIS A and B) may need to continue using stimulation and for them, an implanted stimulator is likely to be convenient. Patients with less disability (AIS C and D) may make useful recovery and improve their quality of life from a course of therapy. This might be locomotion therapy but we argue that cycling with electrical stimulation, which uses biofeedback to encourage descending drive, causes rapid recovery and might be used with little supervision at home, making it much less expensive. Such an electrical therapy followed by conventional physiotherapy might be affordable for the many people living with chronic SCI. To put this in perspective, we present some information about what treatments are funded in the UK and the US.
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Affiliation(s)
- Lynsey D Duffell
- Implanted Devices Group, University College London, London, United Kingdom.,Aspire CREATe, University College London, London, United Kingdom
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7
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Exercise-induced sympathetic dilatation in arterioles of the guinea pig tibial periosteum. Auton Neurosci 2019; 217:7-17. [DOI: 10.1016/j.autneu.2018.12.006] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/13/2018] [Revised: 12/06/2018] [Accepted: 12/21/2018] [Indexed: 11/23/2022]
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Yarar-Fisher C, Polston KFL, Eraslan M, Henley KY, Kinikli GI, Bickel CS, Windham ST, McLain AB, Oster RA, Bamman MM. Paralytic and nonparalytic muscle adaptations to exercise training versus high-protein diet in individuals with long-standing spinal cord injury. J Appl Physiol (1985) 2018; 125:64-72. [PMID: 29494292 PMCID: PMC6086973 DOI: 10.1152/japplphysiol.01029.2017] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2017] [Revised: 01/31/2018] [Accepted: 02/28/2018] [Indexed: 02/08/2023] Open
Abstract
This study compares the effects of an 8-wk isocaloric high-protein (HP) diet versus a combination exercise (Comb-Ex) regimen on paralytic vastus lateralis (VL) and nonparalytic deltoid muscle in individuals with long-standing spinal cord injury (SCI). Fiber-type distribution, cross-sectional area (CSA), levels of translation initiation signaling proteins (Erk-1/2, Akt, p70S6K1, 4EBP1, RPS6, and FAK), and lean thigh mass were analyzed at baseline and after the 8-wk interventions. A total of 11 participants (C5-T12 levels, 21.8 ± 6.3 yr postinjury; 6 Comb-Ex and 5 HP diet) completed the study. Comb-Ex training occurred 3 days/wk and consisted of upper body resistance training (RT) in addition to neuromuscular electrical stimulation (NMES)-induced-RT for paralytic VL muscle. Strength training was combined with high-intensity arm-cranking exercises (1-min intervals at 85-90%, V̇o2peak) for improving cardiovascular endurance. For the HP diet intervention, protein and fat each comprised 30%, and carbohydrate comprised 40% of total energy. Clinical tests and muscle biopsies were performed 24 h before and after the last exercise or diet session. The Comb-Ex intervention increased Type IIa myofiber distribution and CSA in VL muscle and Type I and IIa myofiber CSA in deltoid muscle. In addition, Comb-Ex increased lean thigh mass, V̇o2peak, and upper body strength ( P < 0.05). These results suggest that exercise training is required to promote favorable changes in paralytic and nonparalytic muscles in individuals with long-standing SCI, and adequate dietary protein consumption alone may not be sufficient to ameliorate debilitating effects of paralysis. NEW & NOTEWORTHY This study is the first to directly compare the effects of an isocaloric high-protein diet and combination exercise training on clinical and molecular changes in paralytic and nonparalytic muscles of individuals with long-standing spinal cord injury. Our results demonstrated that muscle growth and fiber-type alterations can best be achieved when the paralyzed muscle is sufficiently loaded via neuromuscular electrical stimulation-induced resistance training.
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Affiliation(s)
- Ceren Yarar-Fisher
- Physical Medicine and Rehabilitation, University of Alabama at Birmingham , Birmingham, Alabama
- University of Alabama at Birmingham Center for Exercise Medicine, University of Alabama at Birmingham , Birmingham, Alabama
| | - Keith F L Polston
- University of Tennessee Health Science Center College of Medicine , Memphis, Tennessee
| | - Mualla Eraslan
- Physical Medicine and Rehabilitation, University of Alabama at Birmingham , Birmingham, Alabama
| | - Kathryn Y Henley
- Physical Medicine and Rehabilitation, University of Alabama at Birmingham , Birmingham, Alabama
| | - Gizem I Kinikli
- Physical Therapy and Rehabilitation, Hacettepe University , Ankara , Turkey
| | - C Scott Bickel
- Physical Therapy and Rehabilitation, Samford University , Birmingham, Alabama
| | - Samuel T Windham
- Department of Surgery, University of Alabama at Birmingham , Birmingham, Alabama
- University of Alabama at Birmingham Center for Exercise Medicine, University of Alabama at Birmingham , Birmingham, Alabama
| | - Amie B McLain
- Physical Medicine and Rehabilitation, University of Alabama at Birmingham , Birmingham, Alabama
- University of Alabama at Birmingham Center for Exercise Medicine, University of Alabama at Birmingham , Birmingham, Alabama
| | - Robert A Oster
- Department of Medicine/Division of Preventive Medicine, University of Alabama at Birmingham , Birmingham, Alabama
| | - Marcas M Bamman
- Department of Cell, Developmental, and Integrative Biology, University of Alabama at Birmingham , Birmingham, Alabama
- University of Alabama at Birmingham Center for Exercise Medicine, University of Alabama at Birmingham , Birmingham, Alabama
- Geriatric Research, Education, and Clinical Center, Birmingham VA Medical Center , Birmingham, Alabama
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O'Brien LC, Wade RC, Segal L, Chen Q, Savas J, Lesnefsky EJ, Gorgey AS. Mitochondrial mass and activity as a function of body composition in individuals with spinal cord injury. Physiol Rep 2017; 5:e13080. [PMID: 28193782 PMCID: PMC5309572 DOI: 10.14814/phy2.13080] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2016] [Accepted: 11/22/2016] [Indexed: 01/02/2023] Open
Abstract
Spinal cord injury (SCI) is accompanied by deterioration in body composition and severe muscle atrophy. These changes put individuals at risk for insulin resistance, type II diabetes, and cardiovascular disease. To determine the relationships between skeletal muscle mitochondrial mass, activity, and body composition, 22 men with motor complete SCI were studied. Body composition assessment was performed using dual-energy X-ray absorptiometry and magnetic resonance imaging. Skeletal muscle biopsies were obtained from the vastus lateralis muscle to measure citrate synthase (CS) and complex III (CIII) activity. CS activity was inversely related to %body fat (r = -0.57, P = 0.013), %leg fat (r = -0.52, P = 0.027), %trunk fat (r = -0.54, P = 0.020), and %android fat (r = -0.54, P = 0.017). CIII activity was negatively related to %body fat (r = -0.58, P = 0.022) and %leg fat (r = -0.54, P = 0.037). Increased visceral adipose tissue was associated with decreased CS and CIII activity (r = -0.66, P = 0.004; r = -0.60, P = 0.022). Thigh intramuscular fat was also inversely related to both CS and CIII activity (r = -0.56, P = 0.026; r = -0.60, P = 0.024). Conversely, lean mass (r = 0.75, P = 0.0003; r = 0.65, P = 0.008) and thigh muscle cross-sectional area (CSA; r = 0.82, P = 0.0001; r = 0.84; P = 0.0001) were positively related to mitochondrial parameters. When normalized to thigh muscle CSA, many body composition measurements remained related to CS and CIII activity, suggesting that %fat and lean mass may predict mitochondrial mass and activity independent of muscle size. Finally, individuals with SCI over age 40 had decreased CS and CIII activity (P = 0.009; P = 0.004), suggesting a decrease in mitochondrial health with advanced age. Collectively, these findings suggest that an increase in adipose tissue and decrease in lean mass results in decreased skeletal muscle mitochondrial activity in individuals with chronic SCI.
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Affiliation(s)
- Laura C O'Brien
- Spinal Cord Injury and Disorders, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
- Department of Physiology and Biophysics, Virginia Commonwealth University, Richmond, Virginia
| | - Rodney C Wade
- Spinal Cord Injury and Disorders, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
| | - Liron Segal
- Spinal Cord Injury and Disorders, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
| | - Qun Chen
- Department of Medicine, Division of Cardiology, Pauley Heart Center Virginia Commonwealth University, Richmond, Virginia
| | - Jeannie Savas
- Department of Surgery, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
- Department of Surgery, Virginia Commonwealth University, Richmond, Virginia
| | - Edward J Lesnefsky
- Department of Physiology and Biophysics, Virginia Commonwealth University, Richmond, Virginia
- Department of Medicine, Division of Cardiology, Pauley Heart Center Virginia Commonwealth University, Richmond, Virginia
- Medical Service, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
- Department of Biochemistry and Molecular Biology, Virginia Commonwealth University, Richmond, Virginia
| | - Ashraf S Gorgey
- Spinal Cord Injury and Disorders, Hunter Holmes McGuire VA Medical Center, Richmond, Virginia
- Physical Medicine and Rehabilitation, Virginia Commonwealth University, Richmond, Virginia
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O’Brien LC, Gorgey AS. Skeletal muscle mitochondrial health and spinal cord injury. World J Orthop 2016; 7:628-637. [PMID: 27795944 PMCID: PMC5065669 DOI: 10.5312/wjo.v7.i10.628] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/05/2016] [Revised: 06/18/2016] [Accepted: 08/15/2016] [Indexed: 02/06/2023] Open
Abstract
Mitochondria are the main source of cellular energy production and are dynamic organelles that undergo biogenesis, remodeling, and degradation. Mitochondrial dysfunction is observed in a number of disease states including acute and chronic central or peripheral nervous system injury by traumatic brain injury, spinal cord injury (SCI), and neurodegenerative disease as well as in metabolic disturbances such as insulin resistance, type II diabetes and obesity. Mitochondrial dysfunction is most commonly observed in high energy requiring tissues like the brain and skeletal muscle. In persons with chronic SCI, changes to skeletal muscle may include remarkable atrophy and conversion of muscle fiber type from oxidative to fast glycolytic, combined with increased infiltration of intramuscular adipose tissue. These changes contribute to a proinflammatory environment, glucose intolerance and insulin resistance. The loss of metabolically active muscle combined with inactivity predisposes individuals with SCI to type II diabetes and obesity. The contribution of skeletal muscle mitochondrial density and electron transport chain activity to the development of the aforementioned comorbidities following SCI is unclear. A better understanding of the mechanisms involved in skeletal muscle mitochondrial dynamics is imperative to designing and testing effective treatments for this growing population. The current editorial will review ways to study mitochondrial function and the importance of improving skeletal muscle mitochondrial health in clinical populations with a special focus on chronic SCI.
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11
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Kent JA, Fitzgerald LF. In vivo mitochondrial function in aging skeletal muscle: capacity, flux, and patterns of use. J Appl Physiol (1985) 2016; 121:996-1003. [PMID: 27539499 DOI: 10.1152/japplphysiol.00583.2016] [Citation(s) in RCA: 28] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2016] [Accepted: 08/17/2016] [Indexed: 01/31/2023] Open
Abstract
Because of the fundamental dependence of mammalian life on adequate mitochondrial function, the question of how and why mitochondria change in old age is the target of intense study. Given the importance of skeletal muscle for the support of mobility and health, this question extends to the need to understand mitochondrial changes in the muscle of older adults, as well. We and others have focused on clarifying the age-related changes in human skeletal muscle mitochondrial function in vivo. These changes include both the maximal capacity for oxidative production of energy (ATP), as well as the relative use of mitochondrial ATP production for powering muscular activity. It has been known for nearly 50 yr that muscle mitochondrial content is highly plastic; exercise training can induce an ∼2-fold increase in mitochondrial content, while disuse has the opposite effect. Here, we suggest that a portion of the age-related changes in mitochondrial function that have been reported are likely the result of behavioral effects, as physical activity influences have not always been accounted for. Further, there is emerging evidence that various muscles may be affected differently by age-related changes in physical activity and movement patterns. In this review, we will focus on age-related changes in oxidative capacity and flux measured in vivo in human skeletal muscle.
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Affiliation(s)
- Jane A Kent
- Muscle Physiology Laboratory, Department of Kinesiology, University of Massachusetts Amherst, Amherst, Massachusetts
| | - Liam F Fitzgerald
- Muscle Physiology Laboratory, Department of Kinesiology, University of Massachusetts Amherst, Amherst, Massachusetts
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12
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Potential of M-Wave Elicited by Double Pulse for Muscle Fatigue Evaluation in Intermittent Muscle Activation by Functional Electrical Stimulation for Motor Rehabilitation. J Med Eng 2016; 2016:6957287. [PMID: 27110556 PMCID: PMC4826699 DOI: 10.1155/2016/6957287] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/16/2015] [Revised: 11/07/2015] [Accepted: 02/28/2016] [Indexed: 11/18/2022] Open
Abstract
Clinical studies on application of functional electrical stimulation (FES) to motor rehabilitation have been increasing. However, muscle fatigue appears early in the course of repetitive movement production training by FES. Although M-wave variables were suggested to be reliable indices of muscle fatigue in long lasting constant electrical stimulation under the isometric condition, the ability of M-wave needs more studies under intermittent stimulation condition, because the intervals between electrical stimulations help recovery of muscle activation level. In this paper, M-waves elicited by double pulses were examined in muscle fatigue evaluation during repetitive movements considering rehabilitation training with surface electrical stimulation. M-waves were measured under the two conditions of repetitive stimulation: knee extension force production under the isometric condition and the dynamic movement condition by knee joint angle control. Amplitude of M-wave elicited by the 2nd pulse of a double pulse decreased during muscle fatigue in both measurement conditions, while the change in M-waves elicited by single pulses in a stimulation burst was not relevant to muscle fatigue in repeated activation with stimulation interval of 1 s. Fatigue index obtained from M-waves elicited by 2nd pulses was suggested to provide good estimation of muscle fatigue during repetitive movements with FES.
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13
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Cisterna BA, Cardozo C, Sáez JC. Neuronal involvement in muscular atrophy. Front Cell Neurosci 2014; 8:405. [PMID: 25540609 PMCID: PMC4261799 DOI: 10.3389/fncel.2014.00405] [Citation(s) in RCA: 40] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/07/2014] [Accepted: 11/10/2014] [Indexed: 12/18/2022] Open
Abstract
The innervation of skeletal myofibers exerts a crucial influence on the maintenance of muscle tone and normal operation. Consequently, denervated myofibers manifest atrophy, which is preceded by an increase in sarcolemma permeability. Recently, de novo expression of hemichannels (HCs) formed by connexins (Cxs) and other none selective channels, including P2X7 receptors (P2X7Rs), and transient receptor potential, sub-family V, member 2 (TRPV2) channels was demonstrated in denervated fast skeletal muscles. The denervation-induced atrophy was drastically reduced in denervated muscles deficient in Cxs 43 and 45. Nonetheless, the transduction mechanism by which the nerve represses the expression of the above mentioned non-selective channels remains unknown. The paracrine action of extracellular signaling molecules including ATP, neurotrophic factors (i.e., brain-derived neurotrophic factor (BDNF)), agrin/LDL receptor-related protein 4 (Lrp4)/muscle-specific receptor kinase (MuSK) and acetylcholine (Ach) are among the possible signals for repression for connexin expression. This review discusses the possible role of relevant factors in maintaining the normal functioning of fast skeletal muscles and suppression of connexin hemichannel expression.
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Affiliation(s)
- Bruno A. Cisterna
- Departamento de Fisiología, Pontificia Universidad Católica de ChileSantiago, Chile
| | - Christopher Cardozo
- Center of Excellence for the Medical Consequences of Spinal Cord Injury, James J. Peters Veterans Affairs Medical CenterBronx, NY, USA
- Departments of Medicine and Rehabilitation Medicine, Icahn School of Medicine at Mount SinaiNew York, NY, USA
| | - Juan C. Sáez
- Departamento de Fisiología, Pontificia Universidad Católica de ChileSantiago, Chile
- Instituto Milenio, Centro Interdisciplinario de Neurociencias de Valparaíso, Universidad de ValparaísoValparaíso, Chile
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Mirbagheri MM, Kindig MW, Niu X. Effects of robotic-locomotor training on stretch reflex function and muscular properties in individuals with spinal cord injury. Clin Neurophysiol 2014; 126:997-1006. [PMID: 25449559 DOI: 10.1016/j.clinph.2014.09.010] [Citation(s) in RCA: 19] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2014] [Revised: 09/03/2014] [Accepted: 09/04/2014] [Indexed: 11/30/2022]
Abstract
OBJECTIVE We sought to determine the therapeutic effect of robotic-assisted step training (RAST) on neuromuscular abnormalities associated with spasticity by characterization of their recovery patterns in people with spinal cord injury (SCI). METHODS Twenty-three motor-incomplete SCI subjects received one-hour RAST sessions three times per week for 4 weeks, while an SCI control group received no training. Neuromuscular properties were assessed using ankle perturbations prior to and during the training, and a system-identification technique quantified stretch reflex and intrinsic stiffness magnitude and modulation with joint position. Growth-mixture modeling classified subjects based on similar intrinsic and reflex recovery patterns. RESULTS All recovery classes in the RAST group presented significant (p<0.05) reductions in intrinsic and reflex stiffness magnitude and modulation with position; the control group presented no changes over time. Subjects with larger baseline abnormalities exhibited larger reductions, and over longer training periods. CONCLUSIONS Our findings demonstrate that RAST can effectively reduce neuromuscular abnormalities, with greater improvements for subjects with higher baseline abnormalities. SIGNIFICANCE Our findings suggest, in addition to its primary goal of improving locomotor patterns, RAST can also reduce neuromuscular abnormalities associated with spasticity. These findings also demonstrate that these techniques can be used to characterize neuromuscular recovery patterns in response to various types of interventions.
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Affiliation(s)
- Mehdi M Mirbagheri
- Department of Physical Medicine and Rehabilitation, Northwestern University, USA; Sensory Motor Performance Program, Rehabilitation Institute of Chicago, USA.
| | - Matthew W Kindig
- Sensory Motor Performance Program, Rehabilitation Institute of Chicago, USA
| | - Xun Niu
- Department of Physical Medicine and Rehabilitation, Northwestern University, USA; Sensory Motor Performance Program, Rehabilitation Institute of Chicago, USA
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15
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Kostovski E, Boon H, Hjeltnes N, Lundell LS, Ahlsén M, Chibalin AV, Krook A, Iversen PO, Widegren U. Altered content of AMP-activated protein kinase isoforms in skeletal muscle from spinal cord injured subjects. Am J Physiol Endocrinol Metab 2013; 305:E1071-80. [PMID: 24022865 DOI: 10.1152/ajpendo.00132.2013] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
AMP-activated protein kinase (AMPK) is a pivotal regulator of energy homeostasis. Although downstream targets of AMPK are widely characterized, the physiological factors governing isoform expression of this protein kinase are largely unknown. Nerve/contractile activity has a major impact on the metabolic phenotype of skeletal muscle, therefore likely to influence AMPK isoform expression. Spinal cord injury represents an extreme form of physical inactivity, with concomitant changes in skeletal muscle metabolism. We assessed the influence of longstanding and recent spinal cord injury on protein abundance of AMPK isoforms in human skeletal muscle. We also determined muscle fiber type as a marker of glycolytic or oxidative metabolism. In subjects with longstanding complete injury, protein abundance of the AMPKγ3 subunit, as well as myosin heavy chain (MHC) IIa and IIx, were increased, whereas abundance of the AMPKγ1 subunit and MHC I were decreased. Similarly, abundance of AMPKγ3 and MHC IIa proteins were increased, whereas AMPKα2, -β1, and -γ1 subunits and MHC I abundance was decreased during the first year following injury, reflecting a more glycolytic phenotype of the skeletal muscle. However, in incomplete cervical lesions, partial recovery of muscle function attenuated the changes in the isoform profile of AMPK and MHC. Furthermore, exercise training (electrically stimulated leg cycling) partly normalized mRNA expression of AMPK isoforms. Thus, physical activity affects the relative expression of AMPK isoforms. In conclusion, skeletal muscle abundance of AMPK isoforms is related to physical activity and/or muscle fiber type. Thus, physical/neuromuscular activity is an important determinant of isoform abundance of AMPK and MCH. This further underscores the need for physical activity as part of a treatment regimen after spinal cord injury to maintain skeletal muscle metabolism.
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Affiliation(s)
- Emil Kostovski
- Section for Spinal Cord Injury, Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway
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16
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Wu Y, Collier L, Qin W, Creasey G, Bauman WA, Jarvis J, Cardozo C. Electrical stimulation modulates Wnt signaling and regulates genes for the motor endplate and calcium binding in muscle of rats with spinal cord transection. BMC Neurosci 2013; 14:81. [PMID: 23914941 PMCID: PMC3735397 DOI: 10.1186/1471-2202-14-81] [Citation(s) in RCA: 23] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/29/2013] [Accepted: 07/19/2013] [Indexed: 01/25/2023] Open
Abstract
BACKGROUND Spinal cord injury (SCI) results in muscle atrophy and a shift of slow oxidative to fast glycolytic fibers. Electrical stimulation (ES) at least partially restores muscle mass and fiber type distribution. The objective of this study was to was to characterize the early molecular adaptations that occur in rat soleus muscle after initiating isometric resistance exercise by ES for one hour per day for 1, 3 or 7 days when ES was begun 16 weeks after SCI. Additionally, changes in mRNA levels after ES were compared with those induced in soleus at the same time points after gastrocnemius tenotomy (GA). RESULTS ES increased expression of Hey1 and Pitx2 suggesting increased Notch and Wnt signaling, respectively, but did not normalize RCAN1.4, a measure of calcineurin/NFAT signaling, or PGC-1ß mRNA levels. ES increased PGC-1α expression but not that of slow myofibrillar genes. Microarray analysis showed that after ES, genes coding for calcium binding proteins and nicotinic acetylcholine receptors were increased, and the expression of genes involved in blood vessel formation and morphogenesis was altered. Of the 165 genes altered by ES only 16 were also differentially expressed after GA, of which 12 were altered in the same direction by ES and GA. In contrast to ES, GA induced expression of genes related to oxidative phosphorylation. CONCLUSIONS Notch and Wnt signaling may be involved in ES-induced increases in the mass of paralyzed muscle. Molecular adaptations of paralyzed soleus to resistance exercise are delayed or defective compared to normally innervated muscle.
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Affiliation(s)
- Yong Wu
- Center of Excellence for the Medical Consequences of SCI, James J. Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
| | - Lauren Collier
- Center of Excellence for the Medical Consequences of SCI, James J. Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
| | - Weiping Qin
- Center of Excellence for the Medical Consequences of SCI, James J. Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
- Department of Medicine, Mount Sinai School of Medicine, New York, NY, USA
| | - Graham Creasey
- VA Palo Alto Health Care System, Stanford University, Palo Alto, CA, USA
| | - William A Bauman
- Center of Excellence for the Medical Consequences of SCI, James J. Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
- Department of Medicine, Mount Sinai School of Medicine, New York, NY, USA
| | - Jonathan Jarvis
- School of Biomedical Sciences, University of Liverpool, Liverpool, UK
| | - Christopher Cardozo
- Center of Excellence for the Medical Consequences of SCI, James J. Peters VA Medical Center, 130 West Kingsbridge Road, Bronx, NY 10468, USA
- Department of Medicine, Mount Sinai School of Medicine, New York, NY, USA
- Department of Rehabilitation Medicine, Mount Sinai School of Medicine, New York, NY, USA
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Ryan TE, Brizendine JT, Backus D, McCully KK. Electrically induced resistance training in individuals with motor complete spinal cord injury. Arch Phys Med Rehabil 2013; 94:2166-73. [PMID: 23816921 DOI: 10.1016/j.apmr.2013.06.016] [Citation(s) in RCA: 51] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/29/2013] [Revised: 06/12/2013] [Accepted: 06/12/2013] [Indexed: 10/26/2022]
Abstract
OBJECTIVE To examine the effects of 16 weeks of electrically induced resistance training on insulin resistance and glucose tolerance, and changes in muscle size, composition, and metabolism in paralyzed muscle. DESIGN Pre-post intervention. SETTING University-based trial. PARTICIPANTS Participants (N=14; 11 men and 3 women) with chronic (>2y post spinal cord injury), motor complete spinal cord injury. INTERVENTION Home-based electrically induced resistance exercise training twice weekly for 16 weeks. MAIN OUTCOME MEASURES Plasma glucose and insulin throughout a standard clinical oral glucose tolerance test, thigh muscle and fat mass via dual-energy x-ray absorptiometry, quadriceps and hamstrings muscle size and composition via magnetic resonance imaging, and muscle oxidative metabolism using phosphorus magnetic resonance spectroscopy. RESULTS Muscle mass increased in all participants (mean ± SD, 39%±27%; range, 5%-84%). The mean change ± SD in intramuscular fat was 3%±22%. Phosphocreatine mean recovery time constants ± SD were 102±24 and 77±18 seconds before and after electrical stimulation-induced resistance training, respectively (P<.05). There was no improvement in fasting blood glucose levels, homeostatic model assessment calculated insulin resistance, 2-hour insulin, or 2-hour glucose. CONCLUSIONS Sixteen weeks of electrical stimulation-induced resistance training increased muscle mass, but did not reduce intramuscular fat. Similarly, factors associated with insulin resistance or glucose tolerance did not improve with training. We did find a 25% improvement in mitochondrial function, as measured by phosphocreatine recovery rates. Larger improvements in mitochondrial function may translate into improved glucose tolerance and insulin resistance.
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Affiliation(s)
- Terence E Ryan
- Department of Kinesiology, University of Georgia, Athens, GA.
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18
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Andrews RK, Schabrun SM, Ridding MC, Galea MP, Hodges PW, Chipchase LS. The effect of electrical stimulation on corticospinal excitability is dependent on application duration: a same subject pre-post test design. J Neuroeng Rehabil 2013; 10:51. [PMID: 23758902 PMCID: PMC3688368 DOI: 10.1186/1743-0003-10-51] [Citation(s) in RCA: 30] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/25/2012] [Accepted: 06/06/2013] [Indexed: 11/10/2022] Open
Abstract
BACKGROUND In humans, corticospinal excitability is known to increase following motor electrical stimulation (ES) designed to mimic a voluntary contraction. However, whether the effect is equivalent with different application durations and whether similar effects are apparent for short and long applications is unknown. The aim of this study was to investigate whether the duration of peripheral motor ES influenced its effect on corticospinal excitability. METHODS The excitability of the corticomotor pathway to abductor pollicis brevis (APB) was measured in fourteen health subjects using transcranial magnetic stimulation before, immediately after and 10 minutes after three different durations (20-, 40-, 60-min) of motor ES (30Hz, ramped). This intervention was designed to mimic a voluntary contraction in APB. To control for effects of motor ES on the peripheral elements (muscle fibre, membrane, neuromuscular junction), maximum compound muscle actions potentials (M-waves) were also recorded at each time point. Results were analysed using a repeated measures analysis of variance. RESULTS Peripheral excitability was reduced following all three motor ES interventions. Conversely, corticospinal excitability was increased immediately following 20- and 40-min applications of motor ES and this increase was maintained at least 20-min following the intervention. A 60-min application of motor ES did not alter corticospinal excitability. CONCLUSIONS A 20-min application of motor ES that is designed to mimic voluntary muscle contraction is as effective as that applied for 40-min when the aim of the intervention is to increase corticospinal excitability. Longer motor ES durations of 60-min do not influence corticospinal excitability, possibly as a result of homeostatic plasticity mechanisms.
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Affiliation(s)
- Rebecca K Andrews
- School of Health and Rehabilitation Sciences and the NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, The University of Queensland, St Lucia, Brisbane, Queensland 4072, Australia
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19
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Primary sensory and motor cortex excitability are co-modulated in response to peripheral electrical nerve stimulation. PLoS One 2012; 7:e51298. [PMID: 23227260 PMCID: PMC3515545 DOI: 10.1371/journal.pone.0051298] [Citation(s) in RCA: 71] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/23/2012] [Accepted: 10/31/2012] [Indexed: 12/03/2022] Open
Abstract
Peripheral electrical stimulation (PES) is a common clinical technique known to induce changes in corticomotor excitability; PES applied to induce a tetanic motor contraction increases, and PES at sub-motor threshold (sensory) intensities decreases, corticomotor excitability. Understanding of the mechanisms underlying these opposite changes in corticomotor excitability remains elusive. Modulation of primary sensory cortex (S1) excitability could underlie altered corticomotor excitability with PES. Here we examined whether changes in primary sensory (S1) and motor (M1) cortex excitability follow the same time-course when PES is applied using identical stimulus parameters. Corticomotor excitability was measured using transcranial magnetic stimulation (TMS) and sensory cortex excitability using somatosensory evoked potentials (SEPs) before and after 30 min of PES to right abductor pollicis brevis (APB). Two PES paradigms were tested in separate sessions; PES sufficient to induce a tetanic motor contraction (30–50 Hz; strong motor intensity) and PES at sub motor-threshold intensity (100 Hz). PES applied to induce strong activation of APB increased the size of the N20-P25 component, thought to reflect sensory processing at cortical level, and increased corticomotor excitability. PES at sensory intensity decreased the size of the P25-N33 component and reduced corticomotor excitability. A positive correlation was observed between the changes in amplitude of the cortical SEP components and corticomotor excitability following sensory and motor PES. Sensory PES also increased the sub-cortical P14-N20 SEP component. These findings provide evidence that PES results in co-modulation of S1 and M1 excitability, possibly due to cortico-cortical projections between S1 and M1. This mechanism may underpin changes in corticomotor excitability in response to afferent input generated by PES.
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20
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Differential expression of caveolins and myosin heavy chains in response to forced exercise in rats. Lab Anim Res 2012; 28:1-9. [PMID: 22474468 PMCID: PMC3315194 DOI: 10.5625/lar.2012.28.1.1] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2011] [Revised: 12/19/2011] [Accepted: 12/19/2011] [Indexed: 11/29/2022] Open
Abstract
Exercise training can improve strength and lead to adaptations in the skeletal muscle and nervous systems. Skeletal muscles can develop into two types: fast and slow, depending on the expression pattern of myosin heavy chain (MHC) isoforms. Previous studies reported that exercise altered the distribution of muscle fiber types. It is not currently known what changes in the expression of caveolins and types of muscle fiber occur in response to the intensity of exercise. This study determined the changes in expression of caveolins and MHC type after forced exercise in muscular and non-muscular tissues in rats. A control (Con) group to which forced exercise was not applied and an exercise (Ex) group to which forced exercise was applied. Forced exercise, using a treadmill, was introduced at a speed of 25 m/min for 30 min, 3 times/day (07:00, 15:00, 23:00). Homogenized tissues were applied to extract of total RNA for further gene analysis. The expression of caveolin-3 and MHC2a in the gastrocnemius muscle of female rats significantly increased in the Ex group compared with the Con group (P<0.05). Furthermore, in the gastrocnemius muscle of male rats, the expression of MHC2x was significantly different between the two groups (P<0.05). There was an increased expression in caveolin-3 and a slightly decreased expression in TGFβ-1 in muscular tissues implicating caveolin-3 influences the expression of MHC isoforms and TGFβ-1 expression. Eventually, it implicates that caveolin-3 has positive regulatory function in muscle atrophy induced by neural dysfunction with spinal cord injury or stroke.
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21
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Chipchase LS, Schabrun SM, Hodges PW. Corticospinal Excitability is Dependent on the Parameters of Peripheral Electric Stimulation: A Preliminary Study. Arch Phys Med Rehabil 2011; 92:1423-30. [DOI: 10.1016/j.apmr.2011.01.011] [Citation(s) in RCA: 64] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/27/2010] [Revised: 01/18/2011] [Accepted: 01/25/2011] [Indexed: 11/25/2022]
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22
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McCully KK, Mulcahy TK, Ryan TE, Zhao Q. Skeletal muscle metabolism in individuals with spinal cord injury. J Appl Physiol (1985) 2011; 111:143-8. [PMID: 21512153 DOI: 10.1152/japplphysiol.00094.2011] [Citation(s) in RCA: 52] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
With increasing survival rates in people with spinal cord injuries (SCI), detection and prevention of metabolic and cardiovascular disease have become increasingly important. Few studies have evaluated in vivo mitochondrial function in paralyzed skeletal muscle. The purpose of this study was to compare oxidative muscle metabolism using the rate of phosphocreatine (PCr) resynthesis measured by magnetic resonance spectroscopy (MRS) in people with SCI and able-bodied (AB) controls. Eight subjects with complete SCI (American Spinal Injury Association Impairment Scale A, levels T3-T12, injury duration 2-13 years) were compared with 12 AB controls. T1-weighted (1)H MR images of the thigh were taken to identify skeletal muscle. Phosphorous MRS was performed with a 13 × 13-cm(2) surface coil placed on the right vastus lateralis in a 3 Tesla clinical MRI scanner. PCr resynthesis was measured after electrical stimulation for 60 s at 4 Hz in SCI and AB and in AB subjects after 39 s of voluntary isometric contractions. Resting metabolites were not different between SCI and AB, except for an elevated phosphodiester peak. PCr recovery was slower in AB subjects using electrical stimulation compared with voluntary exercise (28.4 ± 6.1 vs. 41.5 ± 4.3 s; P < 0.05). PCr recovery rates and calculated muscle maximum oxidative capacity in SCI were both 52% of electrically stimulated AB (P < 0.001). In vivo oxidative metabolism was reduced in paralyzed muscle to a similar extent as seen in people with mitochondrial myopathies and heart failure.
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Affiliation(s)
- Kevin K McCully
- Department of Kinesiology, University of Georgia, 330 River Rd., Athens, GA 30602, USA.
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23
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Duffell LD, Rowlerson AM, Donaldson NDN, Harridge SDR, Newham DJ. Effects of endurance and strength-directed electrical stimulation training on the performance and histological properties of paralyzed human muscle: a pilot study. Muscle Nerve 2010; 42:756-63. [PMID: 20976779 DOI: 10.1002/mus.21746] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022]
Abstract
Electrical stimulation (ES) improves muscle properties after spinal cord injury (SCI), but cycling power output (PO) remains low. We investigated the effect of endurance and strength ES training on these parameters. Assessments of quadriceps strength and fatigue resistance, cycling PO, and muscle biopsies were made in four well-trained SCI subjects (three cyclists and one rower) before and after additional weight training in the cyclists and once in the rower. Weight training improved muscle strength, but cycling PO was low in all subjects. There was no effect of training type on biopsy data. Biopsies showed non-specific signs of pathology, predominance of type IIa fibers, and uniform metabolic activity. Oxidative activity was low, as were capillary:fiber ratios in the cyclists. Cycling PO is limited by factors other than muscle strength. Future ES training studies should attempt to improve muscle oxidative capacity to optimize the potential benefits of ES exercise.
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Affiliation(s)
- Lynsey D Duffell
- Division of Applied Biomedical Research, King's College London, London, UK
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Biering-Sørensen B, Kristensen IB, Kjaer M, Biering-Sørensen F. Muscle after spinal cord injury. Muscle Nerve 2009; 40:499-519. [PMID: 19705475 DOI: 10.1002/mus.21391] [Citation(s) in RCA: 144] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/29/2023]
Abstract
The morphological and contractile changes of muscles below the level of the lesion after spinal cord injury (SCI) are dramatic. In humans with SCI, a fiber-type transformation away from type I begins 4-7 months post-SCI and reaches a new steady state with predominantly fast glycolytic IIX fibers years after the injury. There is a progressive drop in the proportion of slow myosin heavy chain (MHC) isoform fibers and a rise in the proportion of fibers that coexpress both the fast and slow MHC isoforms. The oxidative enzymatic activity starts to decline after the first few months post-SCI. Muscles from individuals with chronic SCI show less resistance to fatigue, and the speed-related contractile properties change, becoming faster. These findings are also present in animals. Future studies should longitudinally examine changes in muscles from early SCI until steady state is reached in order to determine optimal training protocols for maintaining skeletal muscle after paralysis.
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Affiliation(s)
- Bo Biering-Sørensen
- Clinic for Spinal Cord Injuries, NeuroScience Centre, Rigshospitalet, Copenhagen University Hospital, Havnevej 25, DK-3100 Hornbaek, Denmark.
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Duffell LD, Donaldson NDN, Newham DJ. Power Output During Functional Electrically Stimulated Cycling in Trained Spinal Cord Injured People. Neuromodulation 2009; 13:50-7. [DOI: 10.1111/j.1525-1403.2009.00245.x] [Citation(s) in RCA: 15] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
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Duffell LD, de N Donaldson N, Newham DJ. Why is the metabolic efficiency of FES cycling low? IEEE Trans Neural Syst Rehabil Eng 2009; 17:263-9. [PMID: 19258202 DOI: 10.1109/tnsre.2009.2016199] [Citation(s) in RCA: 14] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/08/2022]
Abstract
The potential benefits of functional electrically stimulated (FES) cycling for people with spinal cord injury (SCI) are limited by the power output (PO) attainable. To understand why PO and metabolic efficiency are low, it is helpful to distinguish the effect of the SCI from the effects of electrical stimulation. The purpose of this study was to determine the performance of electrically stimulated (ES) muscle under simpler conditions and in able-bodied people in order to answer two questions about the causes of the poor efficiency in FES cycling. Fifteen able-bodied subjects (26.6 years, six male) performed 5 min of intermittent isometric quadriceps contractions at 40% maximum voluntary contraction during both voluntary and ES activation. Subsequently, nine of them performed 5 min of ES intermittent concentric contractions at the same intensity. This intermittent quadriceps activation imitated the muscles' activity during FES cycling at 35 rpm. Metabolic measurements were recorded. Input power relative to the integral of torque produced (W/Nm x s) was significantly higher during ES than voluntary isometric contractions. Efficiency of ES concentric contractions was 29.6 +/-2.9%. Respiratory exchange ratio was high during ES (1.00-1.01) compared with voluntary (0.91) contractions. ES is less economic than voluntary exercise during isometric contractions, probably due to the greater activation of fast muscle fibres. However, during ES concentric contractions, efficiency is near to the expected values for the velocity chosen. Thus there are additional factors that affect the inefficiency observed during FES cycling.
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Affiliation(s)
- Lynsey D Duffell
- Division of Applied Biomedical Research, King's College London, SE1 1UL London, UK.
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27
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Duffell LD, Donaldson NDN, Perkins TA, Rushton DN, Hunt KJ, Kakebeeke TH, Newham DJ. Long-term intensive electrically stimulated cycling by spinal cord-injured people: Effect on muscle properties and their relation to power output. Muscle Nerve 2008; 38:1304-11. [DOI: 10.1002/mus.21060] [Citation(s) in RCA: 59] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/08/2022]
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28
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DiMarco AF, Kowalski KE. Effects of chronic electrical stimulation on paralyzed expiratory muscles. J Appl Physiol (1985) 2008; 104:1634-40. [PMID: 18403449 DOI: 10.1152/japplphysiol.01321.2007] [Citation(s) in RCA: 14] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Following spinal cord injury, the expiratory muscles develop significant disuse atrophy characterized by reductions in their weight, fiber cross-sectional area, and force-generating capacity. We determined the extent to which these physiological alterations can be prevented with electrical stimulation. Because a critical function of the expiratory muscles is cough generation, an important goal was the maintenance of maximal force production. In a cat model of spinal cord injury, short periods of high-frequency lower thoracic electrical spinal cord stimulation (SCS) at the T(10) level (50 Hz, 15 min, twice/day, 5 days/wk) were initiated 2 wk following spinalization and continued for a 6-mo period. Airway pressure (P)-generating capacity was determined by SCS. Five acute, spinalized animals served as controls. Compared with controls, initial P fell from 43.9 +/- 1.0 to 41.8 +/- 0.7 cmH(2)O (not significant) in the chronic animals. There were small reductions in the weight of the external oblique, internal oblique, transverses abdominis, internal intercostal, and rectus abdominis muscles (not significant for each). There were no significant changes in the population of fast muscle fibers. Because prior studies (Kowalski KE, Romaniuk JR, DiMarco AF. J Appl Physiol 102: 1422-1428, 2007) have demonstrated significant atrophy following spinalization in this model, these results indicate that expiratory muscle atrophy can be prevented by the application of short periods of daily high-frequency stimulation. Because the frequency of stimulation is similar to the expected pattern of clinical use for cough generation, the daily application of electrical stimulation could potentially serve the dual purpose of maintenance of expiratory muscle function and airway clearance.
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Affiliation(s)
- Anthony F DiMarco
- Dept. of Physiology and Biophysics, Case Western Reserve Univ., Cleveland, OH 44109-1998, USA.
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Hafer-Macko CE, Ryan AS, Ivey FM, Macko RF. Skeletal muscle changes after hemiparetic stroke and potential beneficial effects of exercise intervention strategies. JOURNAL OF REHABILITATION RESEARCH AND DEVELOPMENT 2008; 45:261-72. [PMID: 18566944 PMCID: PMC2978978 DOI: 10.1682/jrrd.2007.02.0040] [Citation(s) in RCA: 139] [Impact Index Per Article: 8.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/04/2023]
Abstract
Stroke is the leading cause of disability in the United States. New evidence reveals significant structural and metabolic changes in skeletal muscle after stroke. Muscle alterations include gross atrophy and shift to fast myosin heavy chain in the hemiparetic (contralateral) leg muscle; both are related to gait deficit severity. The underlying molecular mechanisms of this atrophy and muscle phenotype shift are not known. Inflammatory markers are also present in contralateral leg muscle after stroke. Individuals with stroke have a high prevalence of insulin resistance and diabetes. Skeletal muscle is a major site for insulin-glucose metabolism. Increasing evidence suggests that inflammatory pathway activation and oxidative injury could lead to wasting, altered function, and impaired insulin action in skeletal muscle. The health benefits of exercise in disabled populations have now been recognized. Aerobic exercise improves fitness, strength, and ambulatory performance in subjects with chronic stroke. Therapeutic exercise may modify or reverse skeletal muscle abnormalities.
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Kowalski KE, Romaniuk JR, DiMarco AF. Changes in expiratory muscle function following spinal cord section. J Appl Physiol (1985) 2007; 102:1422-8. [PMID: 17158247 DOI: 10.1152/japplphysiol.00870.2006] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Following spinal cord injury, muscles below the level of injury develop variable degrees of disuse atrophy. The present study assessed the physiological changes of the expiratory muscles in a cat model of spinal cord injury. Muscle fiber typing, cross-sectional area, muscle weight, and changes in pressure-generating capacity were assessed in five cats spinalized at the T6level. Airway pressure (P)-generating capacity was monitored during lower thoracic spinal cord stimulation before and 6 mo after spinalization. These parameters were also assessed in five acute animals, which served as controls. In spinalized animals, P fell from 41 ± l to 28 ± 3 cmH2O (means ± SE; P < 0.001). Muscle weight of the external oblique, internal oblique, transversus abdominis, and internal intercostal muscles decreased significantly ( P < 0.05 for each). Muscle weight of the external oblique, internal oblique, transversus abdominis, and internal intercostal, but not rectus abdominis (RA), correlated linearly with P ( r > 0.7 for each; P < 0.05 for each). Mean muscle fiber cross-sectional area of these muscles was significantly smaller ( P < 0.05 for each; except RA) and also correlated linearly with P ( r > 0.55 for each; P < 0.05 for each, except RA). In spinalized animals, the expiratory muscles demonstrated a significant increase in the population of fast muscle fibers. These results indicate that, following spinalization, 1) the expiratory muscles undergo significant atrophy and fiber-type transformation and 2) the P-generating capacity of the expiratory muscles falls significantly secondary to reductions in muscle mass.
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Affiliation(s)
- Krzysztof E Kowalski
- Dept. of Physiology and Biophysics, Case Western Reserve Univ., MetroHealth Medical Center, Rammelkamp Center for Education & Research, 2500 MetroHealth Dr., Cleveland, OH 44109-1998. )
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Malisoux L, Jamart C, Delplace K, Nielens H, Francaux M, Theisen D. Effect of long-term muscle paralysis on human single fiber mechanics. J Appl Physiol (1985) 2006; 102:340-9. [PMID: 17038491 DOI: 10.1152/japplphysiol.00609.2006] [Citation(s) in RCA: 57] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
This study compared human muscles following long-term reduced neuromuscular activity to those with normal functioning regarding single fiber properties. Biopsies were obtained from the vastus lateralis of 5 individuals with chronic (>3 yr) spinal cord injury (SCI) and 10 able-bodied controls (CTRL). Chemically skinned fibers were tested for active and passive mechanical characteristics and subsequently classified according to myosin heavy chain (MHC) content. SCI individuals had smaller proportions of type I (11 +/- 7 vs. 34 +/- 5%) and IIa fibers (11 +/- 6 vs. 31 +/- 5%), whereas type IIx fibers were more frequent (40 +/- 13 vs. 7 +/- 3%) compared with CTRL subjects (P < 0.05). Cross-sectional area and peak force were similar in both groups for all fiber types. Unloaded shortening velocity of fibers from paralyzed muscles was higher in type IIa, IIa/IIx, and IIx fibers (26, 65, and 47%, respectively; P < 0.01). Consequently, absolute peak power was greater in type IIa (46%; P < 0.05) and IIa/IIx fibers (118%; P < 0.01) of the SCI group, whereas normalized peak power was higher in type IIa/IIx fibers (71%; P < 0.001). Ca(2+) sensitivity and passive fiber characteristics were not different between the two groups in any fiber type. Composite values (average value across all fibers analyzed within each study participant) showed similar results for cross-sectional area and peak force, whereas maximal contraction velocity and fiber power were more than 100% greater in SCI individuals. These data illustrate that contractile performance is preserved or even higher in the remaining fibers of human muscles following reduced neuromuscular activity.
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Affiliation(s)
- Laurent Malisoux
- Institut d'Education Physique et de Réadaptation, Faculté de Médecine, Université Catholique de Louvain, Louvain-la-Neuve, Belgium
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Häger-Ross CK, Klein CS, Thomas CK. Twitch and Tetanic Properties of Human Thenar Motor Units Paralyzed by Chronic Spinal Cord Injury. J Neurophysiol 2006; 96:165-74. [PMID: 16611836 DOI: 10.1152/jn.01339.2005] [Citation(s) in RCA: 25] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Little is known about how human motor units respond to chronic paralysis. Our aim was to record surface electromyographic (EMG) signals, twitch forces, and tetanic forces from paralyzed motor units in the thenar muscles of individuals ( n = 12) with chronic (1.5–19 yr) cervical spinal cord injury (SCI). Each motor unit was activated by intraneural stimulation of its motor axon using single pulses and trains of pulses at frequencies between 5 and 100 Hz. Paralyzed motor units ( n = 48) had small EMGs and weak tetanic forces ( n = 32 units) but strong twitch forces, resulting in half-maximal force being achieved at a median of only 8 Hz. The distributions for cumulative twitch and tetanic forces also separated less for paralyzed units than for control units, indicating that increases in stimulation frequency made a smaller relative contribution to the total force output in paralyzed muscles. Paralysis also induced slowing of conduction velocities, twitch contraction times and EMG durations. However, the elevated ratios between the twitch and the tetanic forces, but not contractile speed, correlated significantly with the extent to which unit force summated in response to different frequencies of stimulation. Despite changes in the absolute values of many electrical and mechanical properties of paralyzed motor units, most of the distributions shifted uniformly relative to those of thenar units obtained from control subjects. Thus human thenar muscles paralyzed by SCI retain a population of motor units with heterogeneous contractile properties because chronic paralysis influenced all of the motor units similarly.
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Affiliation(s)
- C K Häger-Ross
- The Miami Project to Cure Paralysis, Department of Neurological Surgery, University of Miami Miller School of Medicine, Miami, FL 33136-2104, USA
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Thijssen DH, Ellenkamp R, Smits P, Hopman MT. Rapid vascular adaptations to training and detraining in persons with spinal cord injury. Arch Phys Med Rehabil 2006; 87:474-81. [PMID: 16571385 DOI: 10.1016/j.apmr.2005.11.005] [Citation(s) in RCA: 59] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2005] [Revised: 10/31/2005] [Accepted: 11/04/2005] [Indexed: 11/18/2022]
Abstract
OBJECTIVE To assess the time course of arterial adaptations during 6 weeks of functional electric stimulation (FES) training and 6 weeks of detraining in subjects with spinal cord injury (SCI). DESIGN Intervention study (before-after trial). SETTING University medical center. PARTICIPANTS Volunteer sample of 9 subjects with SCI. INTERVENTIONS Six weeks of twice weekly FES cycling and 6 weeks of detraining. MAIN OUTCOME MEASURES Vascular characteristics were measured by plethysmography (baseline and peak blood flow of the thigh) and echo Doppler (diameter of the femoral artery and flow-mediated dilation [FMD]). RESULTS After 2 weeks of FES training, arterial characteristics changed significantly; there was an increase in baseline and peak blood flow, an increase in femoral artery diameter, and a decrease in FMD of the femoral artery. Detraining reversed baseline and peak thigh blood flow, vascular resistance, and femoral diameter toward pretraining values within 1 week. However, detraining did not restore the FMD of the femoral artery, even after 6 weeks. CONCLUSIONS Two weeks of hybrid FES training (4 exercise bouts) is sufficient to improve peak leg blood flow and arterial diameter, and to normalize FMD. In addition, detraining results in rapidly reversed vascular characteristics within 1 week.
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Affiliation(s)
- Dick H Thijssen
- Department of Physiology, Institute for Fundamental and Clinical Human Movement Sciences, the Netherlands
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Abstract
Weakness is a characteristic of muscles influenced by the postpolio syndrome (PPS), amyotrophic lateral sclerosis (ALS), and spinal cord injury (SCI). The strength deficits relate to changes in muscle use and to the chronic denervation that can follow the spinal motoneuron death common to these disorders. PPS, ALS, and SCI also involve variable amounts of supraspinal neuron death, the effects of which on muscle weakness remains unclear. Nevertheless, weakness of muscle itself defines the functional consequences of these disorders. A weaker muscle requires an individual to work that muscle at higher than usual intensities relative to its maximal capacity, inducing progressive fatigue and an increased sense of effort. Little evidence is available to suggest that the fatigue commonly experienced by individuals with these disorders relates to an increase in the intrinsic fatigability of the muscle fibers. The only exception is when SCI induces chronic muscle paralysis. To reduce long-term functional deficits in these disorders, studies must identify the signaling pathways that influence neuron survival and determine the factors that encourage and limit sprouting of motor axons. This may ensure that a greater proportion of the fibers in each muscle remain innervated and available for use.
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Affiliation(s)
- Christine K Thomas
- The Miami Project to Cure Paralysis, Lois Pope LIFE Center, 1095 NW 14th Terrace (R-48), Department of Neurological Surgery, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
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Klein CS, Häger-Ross CK, Thomas CK. Fatigue properties of human thenar motor units paralysed by chronic spinal cord injury. J Physiol 2006; 573:161-71. [PMID: 16513673 PMCID: PMC1779696 DOI: 10.1113/jphysiol.2005.103044] [Citation(s) in RCA: 20] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/08/2022] Open
Abstract
Human muscles paralysed chronically by spinal cord injury (SCI) fatigue excessively. Whether these reductions in force reflect a decrease in the fatigue resistance of the motor units is unknown. Our aim was to determine the fatigability of thenar motor units paralysed chronically (10 +/- 2 years) by cervical SCI. Surface electromyographic activity (EMG) and force were recorded from 17 paralysed motor units (n = 7 subjects) in response to intraneural motor axon stimulation (13 pulses at 40 Hz, 1 s(-1) for 2 min). Unit force decreased progressively, reaching 8-60% of initial after 2 min, whereas both the amplitude and area of the first EMG potentials in the trains increased significantly (both P < 0.05). Thus, transmission of neural signals to the sarcolemma was effective and the reduction in force must reflect impaired processes in the muscle fibres. The median fatigue index for paralysed units (0.31), the ratio of the force at 2 min compared to the initial force, was significantly lower than that for units from control subjects (0.85, P < 0.05), but the distribution of fatigue indices for each population had a similar shape (ranges: 0.08-0.60 and 0.41-0.95, respectively). Hence, chronic paralysis did not limit the range of fatigability typically found for thenar units, only its magnitude. These findings suggest that all paralysed units underwent similar reductions in fatigue resistance. After fatigue, paralysed unit forces were reduced at all frequencies (1-100 Hz, P < 0.05). Twitch contraction and half-relaxation times were increased, as was the frequency needed to produce half maximal force (P < 0.05). Thus, stimulation protocols used to produce functional movements in paralysed muscles need to accommodate the significant and rapid fatigue of the motor units.
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Affiliation(s)
- C S Klein
- The Miami Project to Cure Paralysis, Department of Neurological Surgery, University of Miami Miller School of Medicine, 1095 NW 14 Terrace, R48, Miami, FL 33136-2104, USA
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Adams MM, Ditor DS, Tarnopolsky MA, Phillips SM, McCartney N, Hicks AL. The effect of body weight-supported treadmill training on muscle morphology in an individual with chronic, motor-complete spinal cord injury: A case study. J Spinal Cord Med 2006; 29:167-71. [PMID: 16739562 PMCID: PMC1864805 DOI: 10.1080/10790268.2006.11753860] [Citation(s) in RCA: 27] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 10/21/2022] Open
Abstract
OBJECTIVE The purpose of this pilot study was to examine the effects of 4 months of thrice-weekly body weight-supported treadmill training (BWSTT) on skeletal muscle morphology in a woman (age 27 y) with chronic, motor-complete (ASIA B) spinal cord injury (SCI). METHODS The participant performed passive thrice-weekly BWSTT for 4 months (48 total sessions) with manual assistance from therapists. Muscle biopsies of the vastus lateralis were taken prior to the beginning of the training program as well as following the completion of 4 months of training. Histochemical analysis was utilized to evaluate changes in muscle fiber size and type following training. RESULTS At baseline, vastus lateralis muscle biopsies showed evidence of fiber atrophy and fiber type redistribution typical of persons with SCI, with mean fiber areas (and % distributions) of type I, type IIa and type IIx fibers being 3474 microm2 (1.3%), 3146 microm2 (30.8%) and 1284 microm2 (68.0%), respectively. Following training, there were increases in treadmill walking speed (pre: 1.0km/h; post: 2.5km/h) and distance walked/session (pre: 500m; post: 1875m). Vastus lateralis mean fiber area increased by 27.1% and type I fiber % distribution increased to 24.6%, whereas type IIa and type IIx fiber % distributions both decreased following training. CONCLUSION These data indicate that 4 months of thrice-weekly BWSTT improved muscle morphology in an individual with chronic, motor-complete SCI.
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Affiliation(s)
- Melanie M Adams
- Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada.
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Thompson AK, Doran B, Stein RB. Short-term effects of functional electrical stimulation on spinal excitatory and inhibitory reflexes in ankle extensor and flexor muscles. Exp Brain Res 2005; 170:216-26. [PMID: 16317575 DOI: 10.1007/s00221-005-0203-y] [Citation(s) in RCA: 37] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/15/2005] [Accepted: 08/18/2005] [Indexed: 11/27/2022]
Abstract
The purpose of this study was to investigate short-term effects of walking with functional electrical stimulation (FES) on inhibitory and excitatory spinal reflexes in healthy subjects. The FES was applied to the common peroneal (CP) nerve during the swing phase of the step cycle when the ankle flexors are active. We have previously shown that corticospinal excitability for the tibialis anterior (TA) muscle increased after 30 min of FES-assisted walking. An increase of corticospinal excitability could be due to the changes in spinal and/or cortical excitability. Thus, we wished to examine whether a short-term application of FES would increase spinal motoneuronal excitability. Changes could also result from effects on inhibitory as well as excitatory pathways, but to our knowledge no studies have investigated short-term effects of FES on spinal inhibitory pathways. Therefore, we measured reciprocal and presynaptic inhibition, as well as reflex excitability, before and after FES-assisted walking. As controls, effects of FES-like stimulation at rest and walking without stimulation were tested in separate sessions. The TA H-reflex amplitude did not increase after FES in any of the conditions tested, so we have no evidence that FES increases spinal excitability for the TA. The soleus H-reflex decreased slightly (10%) after FES-assisted walking, and remained decreased for at least 30 min. However, the control experiment indicated that this decrease was associated with walking and not with stimulation. Thirty minutes of FES did not produce any significant effects on spinal inhibitory pathways examined in the present study. In conclusion, the soleus H-reflex showed a small but consistent decrease and no spinal circuits examined showed an increase, as was observed in the corticospinal excitability. Thus, we suggest that a short-term application of FES increases the excitability of the cortex or its connections to the spinal cord more effectively than that of spinal pathways.
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Affiliation(s)
- Aiko K Thompson
- Centre for Neuroscience and Department of Physiology, University of Alberta, 513 Heritage Medical Research Centre, Edmonton, AB, T6G 2S2, Canada
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Kebaetse MB, Lee SC, Johnston TE, Binder-Macleod SA. Strategies That Improve Paralyzed Human Quadriceps Femoris Muscle Performance During Repetitive, Nonisometric Contractions. Arch Phys Med Rehabil 2005; 86:2157-64. [PMID: 16271564 DOI: 10.1016/j.apmr.2005.06.011] [Citation(s) in RCA: 25] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/14/2005] [Revised: 05/25/2005] [Accepted: 06/14/2005] [Indexed: 10/25/2022]
Abstract
OBJECTIVE To determine the effect of combining different stimulation frequencies on the ability of paralyzed human quadriceps muscle to produce a 50 degrees knee excursion repetitively when starting at 90 degrees of flexion. DESIGN Repeated-measures design. SETTING Clinical research laboratory. PARTICIPANTS Complete data were collected from 9 subjects aged 11 to 25 years (mean +/- standard deviation, 17.1+/-4.5y) with spinal cord injury (SCI). INTERVENTION Three protocols were each tested during separate sessions: 20-Hz trains of pulses followed by 66-Hz trains (C20+66), 33-Hz trains followed by 66-Hz trains (C33+66), and 66-Hz trains alone (C66). For each frequency, stimulation was repeated until the knee failed to produce a 50 degrees excursion. This approach allowed us to evaluate the response to stimulation with 20-, 33-, and 66-Hz and combinations of 20- and 66-Hz and 33- and 66-Hz trains. MAIN OUTCOME MEASURE Number of successful contractions. RESULTS The C20 and C33 did not differ (mean, 41.0+/-12.6 excursions and 42.0+/-12.3 excursions, respectively), and each produced more excursions than the C66 protocol. The C20+66 and C33+66 protocols produced 51.4+/-15.0 and 44.9+/-13.6 excursions, respectively, and the C20+66 was the best protocol overall (all P<or=.05). CONCLUSIONS This study showed that stimulation strategies that start with low frequencies and switch to higher frequencies as the muscle fatigues could improve the ability of functional electric stimulation applications to perform repetitive, nonisometric contractions in subjects with SCI.
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Affiliation(s)
- Maikutlo B Kebaetse
- Graduate Program in Biomechanics, University of Delaware, Newark, DE 19716, USA
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Vissing K, Andersen JL, Harridge SDR, Sandri C, Hartkopp A, Kjaer M, Schjerling P. Gene expression of myogenic factors and phenotype-specific markers in electrically stimulated muscle of paraplegics. J Appl Physiol (1985) 2005; 99:164-72. [PMID: 15746295 DOI: 10.1152/japplphysiol.01172.2004] [Citation(s) in RCA: 18] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
The transcription factors myogenin and MyoD have been suggested to be involved in maintaining slow and fast muscle-fiber phenotypes, respectively, in rodents. Whether this is also the case in human muscle is unknown. To test this, 4 wk of chronic, low-frequency electrical stimulation training of the tibialis anterior muscle of paraplegic subjects were used to evoke a fast-to-slow transformation in muscle phenotype. It was hypothesized that this would result from an upregulation of myogenin and a downregulation of MyoD. The training evoked the expected mRNA increase for slow fiber-specific markers myosin heavy chain I and 3-hydroxyacyl-CoA dehydrogenase A, whereas an mRNA decrease was seen for fast fiber-specific markers myosin heavy chain IIx and glycerol phosphate dehydrogenase. Although the slow fiber-specific markers citrate synthase and muscle fatty acid binding protein did not display a significant increase in mRNA, they did tend to increase. As hypothesized, myogenin mRNA was upregulated. However, contrary to the hypothesis, MyoD mRNA also increased, although later than myogenin. The mRNA levels of the other myogenic regulatory factor family members, myogenic factor 5 and myogenic regulatory factor 4, and the myocyte enhancer factor (MEF) family members, MEF-2A and MEF-2C, did not change. The results indicate that myogenin is indeed involved in the regulation of the slow oxidative phenotype in human skeletal muscle fibers, whereas MyoD appears to have a more complex regulatory function.
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Affiliation(s)
- Kristian Vissing
- Dept. of Molecular Muscle Biology, Copenhagen Muscle Research Centre, Righospitalet, Univ. of Copenhagen, Denmark
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Frey Law LA, Shields RK. Mathematical models use varying parameter strategies to represent paralyzed muscle force properties: a sensitivity analysis. J Neuroeng Rehabil 2005; 2:12. [PMID: 15927064 PMCID: PMC1175855 DOI: 10.1186/1743-0003-2-12] [Citation(s) in RCA: 12] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/22/2004] [Accepted: 05/31/2005] [Indexed: 11/10/2022] Open
Abstract
Background Mathematical muscle models may be useful for the determination of appropriate musculoskeletal stresses that will safely maintain the integrity of muscle and bone following spinal cord injury. Several models have been proposed to represent paralyzed muscle, but there have not been any systematic comparisons of modelling approaches to better understand the relationships between model parameters and muscle contractile properties. This sensitivity analysis of simulated muscle forces using three currently available mathematical models provides insight into the differences in modelling strategies as well as any direct parameter associations with simulated muscle force properties. Methods Three mathematical muscle models were compared: a traditional linear model with 3 parameters and two contemporary nonlinear models each with 6 parameters. Simulated muscle forces were calculated for two stimulation patterns (constant frequency and initial doublet trains) at three frequencies (5, 10, and 20 Hz). A sensitivity analysis of each model was performed by altering a single parameter through a range of 8 values, while the remaining parameters were kept at baseline values. Specific simulated force characteristics were determined for each stimulation pattern and each parameter increment. Significant parameter influences for each simulated force property were determined using ANOVA and Tukey's follow-up tests (α ≤ 0.05), and compared to previously reported parameter definitions. Results Each of the 3 linear model's parameters most clearly influence either simulated force magnitude or speed properties, consistent with previous parameter definitions. The nonlinear models' parameters displayed greater redundancy between force magnitude and speed properties. Further, previous parameter definitions for one of the nonlinear models were consistently supported, while the other was only partially supported by this analysis. Conclusion These three mathematical models use substantially different strategies to represent simulated muscle force. The two contemporary nonlinear models' parameters have the least distinct associations with simulated muscle force properties, and the greatest parameter role redundancy compared to the traditional linear model.
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Affiliation(s)
- Laura A Frey Law
- Graduate Program in Physical Therapy and Rehabilitation Science, 1-252 Medical Education Bldg., The University of Iowa, Iowa City, IA, USA
| | - Richard K Shields
- Graduate Program in Physical Therapy and Rehabilitation Science, 1-252 Medical Education Bldg., The University of Iowa, Iowa City, IA, USA
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Gerrits KH, Maganaris CN, Reeves ND, Sargeant AJ, Jones DA, de Haan A. Influence of knee joint angle on muscle properties of paralyzed and nonparalyzed human knee extensors. Muscle Nerve 2005; 32:73-80. [PMID: 15795891 DOI: 10.1002/mus.20328] [Citation(s) in RCA: 16] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/10/2022]
Abstract
Muscles of individuals with a spinal cord injury (SCI) exhibit an unexpected leftward shift in the force (torque)-frequency relationship. We investigated whether differences in torque-angle relationships between SCI and able-bodied control muscles could explain this shift. Electrically stimulated knee-extensor contractions were obtained at knee flexion angles of between 30 degrees and 90 degrees. Torque-frequency relationships were obtained at 30 degrees, 90 degrees, and optimum angle. Optimum angle was not different between groups but SCI-normalized torques were lower at the extreme angles. At all angles, SCI muscles produced higher relative torques at low stimulation frequencies. Thus, there was no evidence of a consistent change in the length of paralyzed SCI muscles, and the anomalous leftward shift in the torque-frequency relationship was not the result of testing the muscle at a relatively long length. The results provide valuable information about muscle changes occurring in various neurological disorders.
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Affiliation(s)
- Karin H Gerrits
- Institute for Fundamental and Clinical Human Movement Sciences, Vrije University, van der Boechorststraat 9, 1081 BT Amsterdam, The Netherlands
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Maïmoun L, Puech AM, Manetta J, Badiou S, Paris F, Ohanna F, Rossi M, Sultan C. Circulating leptin concentrations can be used as a surrogate marker of fat mass in acute spinal cord injury patients. Metabolism 2004; 53:989-94. [PMID: 15281006 DOI: 10.1016/j.metabol.2004.03.005] [Citation(s) in RCA: 26] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/15/2022]
Abstract
To determine the acute effect of neurological lesion on body composition, plasma leptin level, and the lipid profile, 7 male patients with acute and complete spinal cord injury (SCI) and 9 able-bodied (AB) males were investigated. At 16, 24, 36, and 48 weeks after injury, plasma leptin level and the lipid profile were analyzed, while whole body (WB) and regional fat mass (FM) and fat-free soft tissue (FFST) were measured by dual-energy x-ray absorptiometry (DXA). At all stages, despite no difference being found between both groups for body mass index (BMI), SCI patients had higher FM at WB (P < .01), lower (P < .01), and upper limbs (P < .05), while FFST was lower at WB (P < .05) and lower limbs (P < .01). The leptin level increased gradually from week 24 and was higher at weeks 16, 36, and 48 in SCI patients than in AB patients (7.0 +/- 3.9; 9.7 +/- 5.1; 10.6 +/- 5.3, respectively, v 3.5 +/- 2.5 ng. mL(-1)). SCI patients had lower high-density lipoprotein-cholesterol (HDL-C) (P < .05) and apolipoprotein (apo) A1 (P < .01), while no difference was found for total cholesterol (TC), low-density lipoprotein-cholesterol (LDL-C), or ApoB levels. At all stages, leptin was strongly and positively correlated with WB and regional FM % (r > 0.75; P < .05) and with TC, LDL-C, and ApoB levels (r > 0.65; P < .05). Leptin was negatively correlated with FFST and the ApoA1/ApoB ratio (r > -0.75; P < .05). In conclusion, neurological lesion induced an early and acute alteration in body composition and lipid profile. The strong relationship between serum leptin and FM suggests that this hormone can be used as a surrogate marker of FM in acute SCI patients and thus would serve as a good indicator for cardiovascular disease risk.
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Affiliation(s)
- Laurent Maïmoun
- Groupe de Recherche Interdisciplinaire Sur le Métabolisme Osseux, Montpellier, France
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Olive JL, Slade JM, Bickel CS, Dudley GA, McCully KK. Increasing blood flow before exercise in spinal cord-injured individuals does not alter muscle fatigue. J Appl Physiol (1985) 2004; 96:477-82. [PMID: 14506095 DOI: 10.1152/japplphysiol.00577.2003] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Previous studies have shown increased fatigue in paralyzed muscle of spinal cord-injured (SCI) patients (Castro M, Apple D Jr, Hillegass E, and Dudley GA. Eur J Appl Physiol 80: 373-378, 1999; Gerrits H, Hopman MTE, Sargeant A, and de Haan A. Clin Physiol 21: 105-113, 2001). Our purpose was to determine whether the increased muscle fatigue could be due to a delayed rise in blood flow at the onset of exercise in SCI individuals. Isometric electrical stimulation was used to induce fatigue in the quadriceps femoris muscle of seven male, chronic (>1 yr postinjury), complete (American Spinal Injury Association, category A) SCI subjects. Cuff occlusion was used to elevate blood flow before electrical stimulation, and the magnitude of fatigue was compared with a control condition of electrical stimulation without prior cuff occlusion. Blood flow was measured in the femoral artery by Doppler ultrasound. Prior cuff occlusion increased blood flow in the first 30 s of stimulation compared with the No-Cuff condition (1,350 vs. 680 ml/min, respectively; P < 0.001), although blood flow at the end of stimulation was the same between conditions (1,260 ± 140 vs. 1,160 ± 370 ml/min, Cuff and No-Cuff condition, respectively; P = 0.511). Muscle fatigue was not significantly different between prior cuff occlusion and the control condition (32 ± 13 vs. 35 ± 10%; P = 0.670). In conclusion, increased muscle fatigue in SCI individuals is not associated with the prolonged time for blood flow to increase at the onset of exercise.
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Affiliation(s)
- Jennifer L Olive
- Department of Radiology, University of Washington, Seattle, Washington 98195, USA.
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Stewart BG, Tarnopolsky MA, Hicks AL, McCartney N, Mahoney DJ, Staron RS, Phillips SM. Treadmill training-induced adaptations in muscle phenotype in persons with incomplete spinal cord injury. Muscle Nerve 2004; 30:61-8. [PMID: 15221880 DOI: 10.1002/mus.20048] [Citation(s) in RCA: 68] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022]
Abstract
Body weight-supported treadmill (BWST) training has been shown to improve ambulatory capacity in persons with a spinal cord injury (SCI); however, the effect that BWST training has on skeletal muscle phenotype is unknown. We aimed to determine whether 6 months (three sessions/week) of BWST training in neurologically stable persons with a traumatic spinal cord injury (ASIA C) alters skeletal muscle phenotype, ambulatory capacity, and blood lipid profile. Externally supported body weight decreased, and walking velocity and duration of the training sessions increased (all P < 0.05) as a result of training. Muscle biopsies revealed increases in the mean muscle-fiber area of type I and IIa fibers. Training induced a reduction in type IIax/IIx fibers, as well as a decrease in IIX myosin heavy chain, and an increase in type IIa fibers. Maximal citrate synthase and 3-hydroxy-acyl-CoA dehydrogenase activity also increased following training. BWST training brought about reductions in plasma total (-11%) and low-density lipoprotein (-13%) cholesterol. We conclude that, in patients with a spinal cord injury, BWST training is able to induce an increase in muscle fiber size and bring about increases in muscle oxidative capacity. In addition, BWST training can bring about improvements in ambulatory capacity and antiatherogenic changes in blood lipid profile.
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Affiliation(s)
- Brian G Stewart
- Department of Kinesiology, McMaster University, 1280 Main Street W, Hamilton, Ontario L8S 4K1, Canada
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Abstract
Persons with spinal cord injury (SCI) exhibit deficits in volitional motor control and sensation that limit not only the performance of daily tasks but also the overall activity level of these persons. This population has been characterised as extremely sedentary with an increased incidence of secondary complications including diabetes mellitus, hypertension and atherogenic lipid profiles. As the daily lifestyle of the average person with SCI is without adequate stress for conditioning purposes, structured exercise activities must be added to the regular schedule if the individual is to reduce the likelihood of secondary complications and/or to enhance their physical capacity. The acute exercise responses and the capacity for exercise conditioning are directly related to the level and completeness of the spinal lesion. Appropriate exercise testing and training of persons with SCI should be based on the individual's exercise capacity as determined by accurate assessment of the spinal lesion. The standard means of classification of SCI is by application of the International Standards for Classification of Spinal Cord Injury, written by the Neurological Standards Committee of the American Spinal Injury Association. Individuals with complete spinal injuries at or above the fourth thoracic level generally exhibit dramatically diminished cardiac acceleration with maximal heart rates less than 130 beats/min. The work capacity of these persons will be limited by reductions in cardiac output and circulation to the exercising musculature. Persons with complete spinal lesions below the T(10) level will generally display injuries to the lower motor neurons within the lower extremities and, therefore, will not retain the capacity for neuromuscular activation by means of electrical stimulation. Persons with paraplegia also exhibit reduced exercise capacity and increased heart rate responses (compared with the non-disabled), which have been associated with circulatory limitations within the paralysed tissues. The recommendations for endurance and strength training in persons with SCI do not vary dramatically from the advice offered to the general population. Systems of functional electrical stimulation activate muscular contractions within the paralysed muscles of some persons with SCI. Coordinated patterns of stimulation allows purposeful exercise movements including recumbent cycling, rowing and upright ambulation. Exercise activity in persons with SCI is not without risks, with increased risks related to systemic dysfunction following the spinal injury. These individuals may exhibit an autonomic dysreflexia, significantly reduced bone density below the spinal lesion, joint contractures and/or thermal dysregulation. Persons with SCI can benefit greatly by participation in exercise activities, but those benefits can be enhanced and the relative risks may be reduced with accurate classification of the spinal injury.
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Affiliation(s)
- Patrick L Jacobs
- Department of Neurological Surgery, The Miami Project to Cure Paralysis, University of Miami School of Medicine, 1095 Northwest 14th Terrace, Miami, R-48, FL 33136, USA.
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Decherchi P, Dousset E, Marqueste T, Berthelin F, Hug F, Jammes Y, Grélot L. Électromyostimulation et récupération fonctionnelle d’un muscle dénervé. Sci Sports 2003. [DOI: 10.1016/s0765-1597(03)00144-8] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/27/2022]
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Bickel CS, Slade JM, Haddad F, Adams GR, Dudley GA. Acute molecular responses of skeletal muscle to resistance exercise in able-bodied and spinal cord-injured subjects. J Appl Physiol (1985) 2003; 94:2255-62. [PMID: 12611774 DOI: 10.1152/japplphysiol.00014.2003] [Citation(s) in RCA: 77] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Spinal cord injury (SCI) results in muscle atrophy, which contributes to a number of health problems, such as cardiovascular deconditioning, metabolic derangement, and osteoporosis. Electromyostimulation (EMS) holds the promise of ameliorating SCI-related muscle atrophy and, therefore, improving general health. To date, EMS training of long-term SCI subjects has resulted in some muscle hypertrophy but has fallen short of normalizing muscle mass. The aim of this study was to compare the molecular responses of vastus lateralis muscles from able-bodied (AB) and SCI subjects after acute bouts of EMS-induced resistance exercise to determine whether SCI muscles displayed some impairment in response. Analysis included mRNA markers known to be responsive to increased loading in rodent muscles. Muscles of AB and SCI subjects were subjected to EMS-stimulated exercise in two 30-min bouts, separated by a 48-h rest. Needle biopsy samples were obtained 24 h after the second exercise bout. In both the AB and SCI muscles, significant changes were seen in insulin-like growth factor binding proteins 4 and 5, cyclin-dependent kinase inhibitor p21, and myogenin mRNA levels. In AB subjects, the mRNA for mechano-growth factor was also increased. Before exercise, the total RNA concentration of the SCI muscles was less than that of the AB subjects but not different postexercise. The results of this study indicate that acute bouts of resistance exercise stimulate molecular responses in the skeletal muscles of both AB and SCI subjects. The responses seen in the SCI muscles indicate that the systems that regulate these molecular responses are intact, even after extended periods of muscle unloading.
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Affiliation(s)
- C Scott Bickel
- Department of Exercise Science, University of Georgia, Athens, Georgia 30602, USA
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Gerrits HL, Hopman MTE, Offringa C, Engelen BGM, Sargeant AJ, Jones DA, Haan A. Variability in fibre properties in paralysed human quadriceps muscles and effects of training. Pflugers Arch 2003; 445:734-40. [PMID: 12632195 DOI: 10.1007/s00424-002-0997-4] [Citation(s) in RCA: 47] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2002] [Revised: 11/06/2002] [Accepted: 11/26/2002] [Indexed: 11/30/2022]
Abstract
A spinal cord injury usually leads to an increase in contractile speed and fatigability of the paralysed quadriceps muscles, which is probably due to an increased expression of fast myosin heavy chain (MHC) isoforms and reduced oxidative capacity. Sometimes, however, fatigue resistance is maintained in these muscles and also contractile speed is slower than expected. To obtain a better understanding of the diversity of these quadriceps muscles and to determine the effects of training on characteristics of paralysed muscles, fibre characteristics and whole muscle function were assessed in six subjects with spinal cord lesions before and after a 12-week period of daily low-frequency electrical stimulation. Relatively high levels of MHC type I were found in three subjects and this corresponded with a high degree of fusion in 10-Hz force responses (r=0.88). Fatigability was related to the activity of succinate dehydrogenase (SDH) (r=0.79). Furthermore, some differentiation between fibre types in terms of metabolic properties were present, with type I fibres expressing the highest levels of SDH and lowest levels of alpha-glycerophosphate dehydrogenase. After training, SDH activity increased by 76+/-26% but fibre diameter and MHC expression remained unchanged. The results indicate that expression of contractile proteins and metabolic properties seem to underlie the relatively normal functional muscle characteristics observed in some paralysed muscles. Furthermore, training-induced changes in fatigue resistance seem to arise, in part, from an improved oxidative capacity.
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Affiliation(s)
- H L Gerrits
- Institute for Fundamental and Clinical Human Movement Sciences, Vrije University Amsterdam, v/d Boechorststraat 9, 1081 BT Amsterdam, The Netherlands.
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Olive JL, Slade JM, Dudley GA, McCully KK. Blood flow and muscle fatigue in SCI individuals during electrical stimulation. J Appl Physiol (1985) 2003; 94:701-8. [PMID: 12391070 DOI: 10.1152/japplphysiol.00736.2002] [Citation(s) in RCA: 52] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Our purpose was to measure blood flow and muscle fatigue in chronic, complete, spinal cord-injured (SCI) and able-bodied (AB) individuals during electrical stimulation. Electrical stimulation of the quadriceps muscles was used to elicit similar activated muscle mass. Blood flow was measured in the femoral artery by Doppler ultrasound. Muscle fatigue was significantly greater (three- to eightfold, P < or = 0.001) in the SCI vs. the AB individuals. The magnitude of blood flow was not significantly different between groups. A prolonged half-time to peak blood flow at the beginning of exercise (fivefold, P = 0.001) and recovery of blood flow at the end of exercise (threefold, P = 0.009) was found in the SCI vs. the AB group. In conclusion, the magnitude of the muscle blood flow to electrical stimulation was not associated with increased muscle fatigue in SCI individuals. However, the prolonged time to peak blood flow may be an explanation for increased fatigue in SCI individuals.
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Affiliation(s)
- Jennifer L Olive
- Department of Exercise Science, University of Georgia, Athens 30602, USA
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Hartkopp A, Harridge SDR, Mizuno M, Ratkevicius A, Quistorff B, Kjaer M, Biering-Sörensen F. Effect of training on contractile and metabolic properties of wrist extensors in spinal cord-injured individuals. Muscle Nerve 2003; 27:72-80. [PMID: 12508298 DOI: 10.1002/mus.10290] [Citation(s) in RCA: 42] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/09/2022]
Abstract
Paretic human muscle rapidly loses strength and oxidative endurance, and electrical stimulation training may partly reverse this. We evaluated the effects of two training protocols on the contractile and metabolic properties of the wrist extensor in 12 C-5/6 tetraplegic individuals. The wrist extensor muscles were stimulated for 30 min/day, 5 days/week, for 12 weeks, using either a high-resistance (Hr) or a low-resistance (Lr) protocol. Total work output was similar in both protocols. The nontrained arm was used as a control. Maximum voluntary torque increased in the Hr (P < 0.05) but not the Lr group. Electrically stimulated peak tetanic torque at 15 HZ, 30 HZ, and 50 HZ were unchanged in the Lr group and tended to increase only at 15 HZ (P < 0.1) in the Hr group. Resistance to fatigue, however, increased (P < 0.05) in both Hr (42%) and Lr (41%) groups. Muscle metabolism was evaluated by (31)P nuclear magnetic resonance spectroscopy ((31)P-NMRS) during and following a continuous 40-s 10-HZ contraction. In the Hr group the cost of contraction decreased by 38% (P < 0.05) and the half-time of phosphocreatine (PCr) recovery was shortened by 52% (P < 0.05). Thus, long-term electrically induced stimulation of the wrist extensor muscles in spinal cord injury (SCI) increases fatigue resistance independent of training pattern. However, only the Hr protocol increased muscle strength and was shown to improve muscle aerobic metabolism after training. Muscle Nerve 27: 72-80, 2003
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Affiliation(s)
- Andreas Hartkopp
- Clinic for Para- and Tetraplegia, The Neuroscience Centre, Rigshospitalet, Copenhagen University Hospitals, Copehagen, Denmark.
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