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 α-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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Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M (1996) Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflugers Arch 431:513–518
Bottinelli R, Canepari M, Pellegrino MA, Reggiani C (1996) Force-velocity properties of human skeletal muscle fibres: myosin heavy chain isoform and temperature dependence. J Physiol (Lond) 495:573
Brooke MH, Kaiser KK (1970) Muscle fiber types: how many and what kind? Arch Neurol 23:369–79
Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R (1997) Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord 35:86–91
Chilibeck PD, Jeon J, Weiss C, Bell G, Burnham R (1999) Histochemical changes in muscle of individuals with spinal cord injury following functional electrical stimulated exercise training. Spinal Cord. 37:264–268
Demirel HA, Powers SK, Naito H, Hughes M, Coombes JS (1999) Exercise-induced alterations in skeletal muscle myosin heavy chain phenotype: dose-response relationship. J Appl Physiol 86:1002–1008
Gauthier JM, Theriault R, Theriault G, Gelinas Y, Simoneau JA (1992) Electrical stimulation-induced changes in skeletal muscle enzymes of men and women. Med Sci Sports Exerc 24:1252–1256
Gerrits HL, Haan A de, Hopman MTE, Woude LHV van der, Jones DA, Sargeant AJ (1999) Contractile properties of the quadriceps muscle in individuals with spinal cord injury. Muscle Nerve 22:1249–1256
Gerrits HL, Hopman MTE, Sargeant AJ, Jones DA, Haan A de (2002) Effects of training on contractile properties of the paralyzed quadriceps muscle. Muscle Nerve 25:559–567
Harridge SDR, Bottinelli R, Canepari M, et al. (1996) Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflugers Arch 432:913–920
Hartkopp A, Andersen JL, Harridge SD, et al (1999) High expression of MHC I in the tibialis anterior muscle of a paraplegic patient. Muscle Nerve 22:1731–1737
Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol (Lond) 472:595–614
Martin TP, Vailas AC, Durivage JB, Edgerton VR, Castleman KR (1985) Quantitative histochemical determination of muscle enzymes: biochemical verification. J Histochem Cytochem 33:1053–1059
Martin TP, Stein RB, Hoeppner PH, Reid DC (1992) Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol 72:1401–1406
Maynard FM, Jr., Bracken MB, Creasey G, et al (1997) International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 35:266–274
Melichna J, Zauner CW, Havlickova L, Novak J, Hill DW, Colman RJ (1990) Morphologic differences in skeletal muscle with age in normally active human males and their well-trained counterparts. Hum Biol 62:205–220
Pette D (1984) J.B. Wolffe memorial lecture. Activity-induced fast to slow transitions in mammalian muscle. Med Sci Sports Exerc 16:517–528
Pette D, Staron RS (1997) Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170:143–223
Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202
Rochester L, Chandler CS, Johnson MA, Sutton RA, Miller S (1995) Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 1. Contractile properties. Paraplegia 33:437–449
Rochester L, Barron MJ, Chandler CS, Sutton RA, Miller S, Johnson MA (1995) Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 2. Morphological and histochemical properties. Paraplegia 33:514–522
Salmons S (1994) Exercise, stimulation and type transformation of skeletal muscle. Int J Sports Med 15:136–141
Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76:371–423
Simoneau JA, Bouchard C (1989) Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257:E567–E572
Simoneau JA, Lortie G, Boulay MR, Thibault MC, Theriault G, Bouchard C (1985) Skeletal muscle histochemical and biochemical characteristics in sedentary male and female subjects. Can J Physiol Pharmacol 63:30–35
Stein RB, Gordon T, Jefferson J, et al (1992) Optimal stimulation of paralyzed muscle after human spinal cord injury. J Appl Physiol 72:1393–1400
Sweat F, Puchtler H, Rosenthal SI (1964) Sirius red f3ba as a stain for connective tissue. Arch Pathol 78:69–72
Talmadge RJ (2000) Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms. Muscle Nerve 23:661–79
Thériault R, Thériault G, Simoneau JA (1994) Human skeletal muscle adaptation in response to chronic low-frequency electrical stimulation. J Appl Physiol 77:1885–1889
Thériault R, Boulay MR, Thériault G, Simoneau JA (1996) Electrical stimulation-induced changes in performance and fiber type proportion of human knee extensor muscles. Eur J Appl Physiol 74:311–317
Acknowledgements
The present study required a lot of commitment of the SCI subjects performing daily training sessions. Without such commitment this study would not have been possible and we therefore thank all participants. We also gratefully acknowledge Henriette Haan and Ruth v/d Vliet (Vrije University Amsterdam), as well as Petra Habets (Amsterdam Medical Center) and Henk ter Laak (University Medical Center St. Radboud, Nijmegen), for their support during the processing and analyses of the biopsy samples.
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Gerrits, H.L., Hopman, M.T.E., Offringa, C. et al. Variability in fibre properties in paralysed human quadriceps muscles and effects of training. Pflugers Arch - Eur J Physiol 445, 734–740 (2003). https://doi.org/10.1007/s00424-002-0997-4
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DOI: https://doi.org/10.1007/s00424-002-0997-4