Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Acta Neuropathologica
Published in: Acta Neuropathologica 6/2006

01-06-2006 | Original Paper

Chronic electrostimulation after nerve repair by self-anastomosis: effects on the size, the mechanical, histochemical and biochemical muscle properties

Authors: T. Marqueste, P. Decherchi, D. Desplanches, R. Favier, L. Grelot, Y. Jammes

Published in: Acta Neuropathologica | Issue 6/2006

Login to get access

Abstract

This study tests the effects of chronic electrostimulation on denervated/reinnervated skeletal muscle in producing an optimal restoration of size and mechanical and histochemical properties. We compared tibialis anterior muscles in four groups of rats: in unoperated control (C) and 10 weeks following nerve lesion with suture (LS) in the absence of electrostimulation and in the presence of muscle stimulation with either a monophasic rectangular current (LSEm) or a biphasic modulated current (LSEb). The main results were (1) muscle atrophy was reduced in LSEm (−26%) while it was absent in LSEb groups (−8%); (2) the peak twitch amplitude decreased in LS and LSEm but not in LSEb groups, whereas the contraction time was shorter; (3) muscle reinnervation was associated with the emergence of type IIC fibers and proportions of types I, IIA and IIB fibers recovered in the superficial portion of LSEb muscles; (4) the ratio of oxidative to glycolytic activities decreased in the three groups with nerve injury and repair; however, this decrease was more accentuated in LSEm groups. We conclude that muscle electrostimulation following denervation and reinnervation tends to restore size and functional and histochemical properties during reinnervation better than is seen in unstimulated muscle.
Literature
1.
Anderl H (1977) Cross-face nerve transplantation in fascial palsy. Proc R Soc Med 70:143–144PubMed
2.
Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10:153–160PubMed
3.
Bain JR, Veltri KL, Chamberlain D, Fahnestock M (2001) Improved functional recovery of denervated skeletal muscle after temporary sensory nerve innervation. Neuroscience 103:503–510PubMedCrossRef
4.
Balice-Gordon RJ, Thompson WJ (1988) The organization and development of compartmentalized innervation in rat extensor digitorum longus muscle. J Physiol 398:211–231PubMed
5.
Bar A, Pette D (1988) Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett 235(1–2):153–155PubMedCrossRef
6.
Booth FW, Thomason DB (1991) Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev 71:541–585PubMed
7.
Boudriau S, Cote CH, Vincent M, Houle P, Tremblay RR, Rogers PA (1996) Remodeling of the cytoskeletal lattice in denervated skeletal muscle. Muscle Nerve 19:1383–1390CrossRefPubMed
8.
Briggs FN, Poland JL, Solaro RJ (1977) Relative capabilities of sarcoplasmic reticulum in fast and slow mammalian skeletal muscles. J Physiol 266:587–594PubMed
9.
Brooke MH, Kaiser KK (1970) Muscle fiber types: how many and what kind? Arch Neurol 23:369–379PubMed
10.
Brown JM, Henriksson J, Salmons S (1989) Restoration of fast muscle characteristics following cessation of chronic stimulation: physiological, histochemical and metabolic changes during slow-to-fast transformation. Proc R Soc Lond B Biol Sci 235:321–346PubMed
11.
Carlsen RC, Klein HW, Matthews CC, Gourley IM (1987) Recovery of free muscle grafts in rat: improvement is associated with an increase in cyclic adenosine monophosphate concentration or use of the condition/test paradigm. Exp Neurol 98:616–632PubMedCrossRef
12.
Carlson BM, Faulkner JA (1988) Reinnervation of long-term denervated rat muscle freely grafted into an innervated limb. Exp Neurol 102:50–56CrossRefPubMed
13.
Carlson BM, Hnik P, Tucek S, Vejsada R, Bader DM, Faulkner JA (1981) Comparison between grafts with intact nerves and standard free grafts of the rat extensor digitorum longus muscle. Physiol Bohemoslov 30:505–514PubMed
14.
Carlson BM, Billington L, Faulkner J (1996) Studies on the regenerative recovery of long-term denervated muscle in rats. Res Neurol Neurosci 10:77–84
15.
Carraro U, Catani C, Belluco S, Cantini M, Marchioro L (1986) Slow-like electrostimulation switches on slow myosin in denervated fast muscle. Exp Neurol 94:537–553CrossRefPubMed
16.
Carraro U, Catani C, Saggin L, Zrunek M, Szabolcs M, Gruber H, Streinzer W, Mayr W, Thoma H (1988) Isomyosin changes after functional electrostimulation of denervated sheep muscle. Muscle Nerve 11:1016–1028CrossRefPubMed
17.
Chi MM, Hintz CS, Henriksson J, Salmons S, Hellendahl RP, Park JL, Nemeth PM, Lowry OH (1986) Chronic stimulation of mammalian muscle: enzyme changes in individual fibers. Am J Physiol 251:633–642
18.
Close R (1969) Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union. J Physiol 204:331–346PubMed
19.
Csukly K, Marqueste T, Gardiner P (2005) Sensitivity of rat soleus muscle to a mechanical stimulus is decreased following hindlimb unweighting. Eur J Appl Physiol 95(2–3):243–249CrossRefPubMed
20.
Curwin S, Stanish WD, Valiant G (1980) Clinical applications and biochemical effects of high frequency electrical stimulation. Can Athl Trainers Assoc J 6:15–16
21.
Decherchi P, Vuillon-Cacciutolo G, Darques JL, Jammes Y (2001) Changes in afferent activities from tibialis anterior muscle after nerve repair by self-anastomosis. Muscle Nerve 24:59–68CrossRefPubMed
22.
Delp MD, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80:261–270PubMed
23.
Desplanches D, Mayet MH, Sempore B, Flandrois R (1987) Structural and functional responses to prolonged hindlimb suspension in rat muscle. J Appl Physiol 63:558–563PubMed
24.
Eberstein A, Pachter BR (1986) The effect of electrical stimulation on reinnervation of rat muscle: contractile properties and endplate morphometry. Brain Res 384(2):304–310CrossRefPubMed
25.
Eken T, Gundersen K (1988) Electrical stimulation resembling normal motor-unit activity: effects on denervated fast and slow rat muscles. J Physiol 402:651–669PubMed
26.
Eriksson E, Haggmark T (1979) Comparison of isometric muscle training and electrical stimulation supplementing isometric muscle training in the recovery after major knee ligament surgery. A preliminary report. Am J Sports Med 7:169–171PubMedCrossRef
27.
Esau SA, Bellemare F, Grassino A, Permutt S, Roussos C, Pardy RL (1983) Changes in relaxation rate with diaphragmatic fatigue in humans. J Appl Physiol 54:1353–1360PubMed
28.
Faucher M, Guillot C, Marqueste T, Kipson N, Mayet-Sornay MH, Desplanches D, Jammes Y, Badier M (2005) Matched adaptations of electrophysiological, physiological, and histological properties of skeletal muscles in response to chronic hypoxia. Pflugers Arch 450:45–52CrossRefPubMed
29.
Gatchalian CL, Schachner M, Sanes JR (1989) Fibroblasts that proliferate near denervated synaptic sites in skeletal muscle synthesize the adhesive molecules tenascin(J1), N-CAM, fibronectin, and a heparan sulfate proteoglycan. J Cell Biol 108:873–1890CrossRef
30.
Gillespie MJ, Gordon T, Murphy PR (1987) Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation. J Neurophysiol 57:921–937PubMed
31.
Goldspink G (1999) Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194:323–334CrossRefPubMed
32.
Goldspink G, Yang SY (2001) Effects of activity on growth factor expression. Int J Sport Nutr Exerc Metab 11:21–27
33.
Gordon T, Mao J (1994) Muscle atrophy and procedures for training after spinal cord injury. Phys Ther 74:50–60PubMed
34.
Gorza L, Gundersen K, Lomo T, Schiaffino S, Westgaard RH (1988) Slow-to-fast transformation of denervated soleus muscles by chronic high-frequency stimulation in the rat. J Physiol 402:627–649PubMed
35.
Grandmontagne M, Vaage O, Kopke Vollestad N, Hermansen L (1982) Confrontation de methods histochimiques et d’immunofluorescence pour le typage des fibres du muscle squelettique de rat (Abstract). J Physiol Paris 78:14A
36.
Graziotti GH, Rios CM, Rivero JL (2001) Evidence for three fast myosin heavy chain isoforms in type II skeletal muscle fibers in the adult llama (Lama glama). J Histochem Cytochem 49:1033–1044PubMed
37.
Green HJ, Klug GA, Reichmann H, Seedorf U, Wiehrer W, Pette D (1984) Exercise-induced fibre type transitions with regard to myosin, parvalbumin, and sarcoplasmic reticulum in muscles of the rat. Pflugers Arch 400:432–438CrossRefPubMed
38.
Green HJ, Reichmann H, Pette D (1984) Inter- and intraspecies comparisons of fibre type distribution and of succinate dehydrogenase activity in type I, IIA and IIB fibres of mammalian diaphragms. Histochemistry 81:67–73CrossRefPubMed
39.
Gulati AK (1988) Long-term retention of regenerative capability after denervation of skeletal muscle, and dependency of late differentiation on innervation. Anat Rec 220:429–434CrossRefPubMed
40.
Gundersen K (1998) Determination of muscle contractile properties: the importance of the nerve. Acta Physiol Scand 162:333–341CrossRefPubMed
41.
Gundersen K, Leberer E, Lomo T, Pette D, Staron RS (1988) Fibre types, calcium-sequestering proteins and metabolic enzymes in denervated and chronically stimulated muscles of the rat. J Physiol 398:177–189PubMed
42.
Guth L, Samaha FJ (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. Exp Neurol 25:138–152CrossRefPubMed
43.
Gutmann E (ed) (1962) The denervated muscle. Czechoslovak Academy of Sciences, Praha
44.
Gutmann E (1973) Basic mechanisms and effects of muscular activity and inactivity. Fysiatr Revmatol Vestn 51:125–127PubMed
45.
Hamalainen N, Pette D (1996) Slow-to-fast transitions in myosin expression of rat soleus muscle by phasic high-frequency stimulation. FEBS Lett 399:220–222CrossRefPubMed
46.
47.
Hennig R, Lomo T (1987) Effects of chronic stimulation on the size and speed of long-term denervated and innervated rat fast and slow skeletal muscles. Acta Physiol Scand 130:115–131PubMed
48.
Henriksson J, Chi MM, Hintz CS, Young DA, Kaiser KK, Salmons S, Lowry OH (1986) Chronic stimulation of mammalian muscle: changes in enzymes of six metabolic pathways. Am J Physiol 251:614–632
49.
Hintz CS, Coyle EF, Kaiser KK, Chi MM, Lowry OH (1984) Comparison of muscle fiber typing by quantitative enzyme assays and by myosin ATPase staining. J Histochem Cytochem 32:655–660PubMed
50.
Jakubiec-Puka A, Kordowska J, Catani C, Carraro U (1990) Myosin heavy chain isoform composition in striated muscle after denervation and self-reinnervation. Eur J Biochem 193:623–628PubMedCrossRef
51.
Jakubiec-Puka A, Ciechomska I, Morga J, Matusiak A (1999) Contents of myosin heavy chains in denervated slow and fast rat leg muscles. Comp Biochem Physiol B Biochem Mol Biol 122:355–362CrossRefPubMed
52.
Jammes Y, Collett P, Lenoir P, Lama A, Berthelin F, Roussos C (1991) Diaphragmatic fatigue produced by constant or modulated electric currents. Muscle Nerve 14:27–34CrossRefPubMed
53.
Jarvis JC, Sutherland H, Mayne CN, Gilroy SJ, Salmons S (1996) Induction of a fast-oxidative phenotype by chronic muscle stimulation: mechanical and biochemical studies. Am J Physiol 270:306–312
54.
Kanaya F, Tajima T (1992) Effect of electrostimulation on denervated muscle. Clin Orthop Relat Res Oct:296–301
55.
Kern H, Boncompagni S, Rossini K, Mayr W, Fano G, Zanin ME, Podhorska-Okolow M, Protasi F, Carraro U (2004) Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? Neuropathol Exp Neurol 63(9):919–931
56.
Klein HW, Carlsen RC, Gourley I (1988) Pharmacologic enhancement of functional recovery in free muscle transfers. J Reconstr Microsurg 4:277–281, 283–284
57.
Kostyukov AI, Hellstrom F, Korchak OE, Radovanovic S, Ljubisavljevic M, Windhorst U, Johansson H (2000) Fatigue effects in the cat gastrocnemius during frequency-modulated efferent stimulation. Neuroscience 97:789–799PubMedCrossRef
58.
LaFramboise WA, Daood MJ, Guthrie RD, Moretti P, Schiaffino S, Ontell M (1990) Electrophoretic separation and immunological identification of type 2X myosin heavy chain in rat skeletal muscle. Biochim Biophys Acta 1035:109–112PubMed
59.
Lopez-Guajardo A, Sutherland H, Jarvis JC, Salmons S (2000) Dynamics of stimulation-induced muscle adaptation: insights from varying the duty cycle. J Muscle Res Cell Motil 21:725–735CrossRefPubMed
60.
Lopez-Guajardo A, Sutherland H, Jarvis JC, Salmons S (2001) Induction of a fatigue-resistant phenotype in rabbit fast muscle by small daily amounts of stimulation. J Appl Physiol 90:1909–1918PubMed
61.
Love FM, Son YJ, Thompson WJ (2003) Activity alters muscle reinnervation and terminal sprouting by reducing the number of Schwann cell pathways that grow to link synaptic sites. J Neurobiol 54(4):566–576PubMedCrossRef
62.
Lowry OH, Passonneau JV (ed) (1972) A flexible system of enzymatic analysis. Academic Press, New York
63.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMed
64.
Marqueste T, Decherchi P, Dousset E, Berthelin F, Jammes Y (2002) Effect of muscle electrostimulation on afferent activities from tibialis anterior muscle after nerve repair by self-anastomosis. Neuroscience 113:257–271PubMedCrossRef
65.
Marqueste T, Hug F, Decherchi P, Jammes Y (2003) Changes in neuromuscular function after training by functional electrical stimulation. Muscle Nerve 28(2):181–188CrossRefPubMed
66.
Marqueste T, Alliez JR, Alluin O, Jammes Y, Decherchi P (2004) Neuromuscular rehabilitation by treadmill running or electrical stimulation after peripheral nerve injury and repair. J Appl Physiol 96:1988–1995CrossRefPubMed
67.
Mayne CN, Sutherland H, Jarvis JC, Gilroy SJ, Craven AJ, Salmons S (1996) Induction of a fast-oxidative phenotype by chronic muscle stimulation: histochemical and metabolic studies. Am J Physiol 270:313–320
68.
McKoy G, Ashley W, Mander J, Yang SY, Williams N, Russell B, Goldspink G (2002) Expression of insulin growth factor-1 splice variants and structural genes in rabbit skeletal muscle induced by stretch and stimulation. J Physiol 516:583–592CrossRef
69.
Mira JC, Janmot C, Couteaux R, d’Albis A (1992) Reinnervation of denervated extensor digitorum longus of the rat by the nerve of the soleus does not induce the type I myosin synthesis directly but through a sequential transition of type II myosin isoforms. Neurosci Lett 141:223–226CrossRefPubMed
70.
Pachter BR, Eberstein A (1983) Endplate postsynaptic structure dependent upon muscle activity. Neurosci Lett 43(2–3):277–283CrossRefPubMed
71.
Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50:500–509CrossRefPubMed
72.
Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202PubMed
73.
Pette D, Muller W, Leisner E, Vrbova G (1976) Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscles of the rabbit. Pflugers Arch 364:103–112CrossRefPubMed
74.
Pierobon-Bormioli S, Sartore S, Libera LD, Vitadello M, Schiaffino S (1987) “Fast” isomyosins and fiber types in mammalian skeletal muscle. J Histochem Cytochem 29:1179–1188
75.
Reichmann H, Nix WA (1985) Changes of energy metabolism, myosin light chain composition, lactate dehydrogenase isozyme pattern and fibre type distribution of denervated fast-twitch muscle from rabbit after low frequency stimulation. Pflugers Arch 405:244–249CrossRefPubMed
76.
Reichmann H, Srihari T, Pette D (1983) Ipsi- and contralateral fibre transformations by cross-reinnervation. A principle of symmetry. Pflugers Arch 397:202–208CrossRefPubMed
77.
Rosser BW, Norris BJ, Nemeth PM (1992) Metabolic capacity of individual muscle fibers from different anatomic locations. J Histochem Cytochem 40:819–825PubMed
78.
Sakakima H, Yoshida Y (2003) Effects of short duration static stretching on the denervated and reinnervated soleus muscle morphology in the rat. Arch Phys Med Rehabil 84(9):1339–1342CrossRefPubMed
79.
Salmons S, Sreter FA (1976) Significance of impulse activity in the transformation of skeletal muscle type. Nature 263:30–34CrossRefPubMed
80.
Salmons S, Ashley Z, Sutherland H, Russold MF, Li F, Jarvis JC (2005) Functional electrical stimulation of denervated muscles: basic issues. Artif Organs 29(3):199–202CrossRefPubMed
81.
Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205CrossRefPubMed
82.
Siironen J, Sandberg M, Vuorinen V, Roytta M (1992) Expression of type I and III collagens and fibronectin after transection of rat sciatic nerve. Reinnervation compared with denervation. Lab Invest 67:80–87PubMed
83.
84.
Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos GE (1999) Fiber type composition of four hindlimb muscles of adult Fisher 344 rats. Histochem Cell Biol 111:117–123CrossRefPubMed
85.
Sunderland S (1978) Nerve and nerve injuries, 2nd edn. Churchill-Livingston, Edinburgh
86.
Terzis J, Faibisoff B, Williams B (1975) The nerve gap: suture under tension vs. graft. Plast Reconstr Surg 56:166–170PubMedCrossRef
87.
Thomas CK, Nelson G, Than L, Zijdewind I (2002) Motor unit activation order during electrically evoked contractions of paralyzed or partially paralyzed muscles. Muscle Nerve 25:797–804CrossRefPubMed
88.
Totosy de Zepetnek JE, Zung HV, Erdebil S, Gordon T (1992) Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. J Neurophysiol 67:1404–1415
89.
Ullman M, Alameddine H, Skottner A, Oldfors A (1989) Effects of growth hormone on skeletal muscle. II. Studies on regeneration and denervation in adult rats. Acta Physiol Scand 135:537–543PubMed
90.
Virtanen P, Tolonen U, Savolainen J, Takala TE (1992) Effect of reinnervation on collagen synthesis in rat skeletal muscle. J Appl Physiol 72:2069–2074CrossRefPubMed
91.
Vuillon-Cacciuttolo G, Berthelin F, Jammes Y (1997) Dissociated changes in fatigue resistance and characteristics of M waves and twitches in a fast muscle group after two weeks of chronic stimulation: influence of the stimulation patterns. Muscle Nerve 20:604–607CrossRefPubMed
92.
Wang LC, Kernell D (2002) Recovery of type I fiber regionalization in gastrocnemius medialis of the rat after reinnervation along original and foreign paths, with and without muscle rotation. Neuroscience 114:629–640PubMedCrossRef
93.
Wang L, Copray S, Brouwer N, Meek MF, Kernell D (2002) Regional distribution of slow-twitch muscle fibers after reinnervation in adult rat hindlimb muscles. Muscle Nerve 25:805–815CrossRefPubMed
94.
Westgaard RH, Lomo T (1988) Control of contractile properties within adaptive ranges by patterns of impulse activity in the rat. J Neurosci 8:4415–4426PubMed
95.
White TP, Devor S (1993) Skeletal muscle regeneration and plasticity of grafts. In: Holloszy J (ed) Exercise and sport sciences reviews, vol 21, pp 263–295
96.
Windisch A, Gundersen K, Szabolcs MJ, Gruber H, Lomo T (1998) Fast to slow transformation of denervated and electrically stimulated rat muscle. J Physiol 510:623–632CrossRefPubMed
97.
Yang S, Alnaqeeb M, Simpson H, Goldspink G (1996) Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J Muscle Res Cell Motil 17:487–495CrossRefPubMed
Metadata
Title
Chronic electrostimulation after nerve repair by self-anastomosis: effects on the size, the mechanical, histochemical and biochemical muscle properties
Authors
T. Marqueste
P. Decherchi
D. Desplanches
R. Favier
L. Grelot
Y. Jammes
Publication date
01-06-2006
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 6/2006
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-006-0035-2

Other articles of this Issue 6/2006

Acta Neuropathologica 6/2006 Go to the issue

Original Paper

Regulation of microglial cell responses in murine Toxoplasma encephalitis by CD200/CD200 receptor interaction

Original Paper

Cytogenetic features of ependymoblastomas

Original Paper

Functional recovery improvement is related to aberrant reinnervation trimming. A comparative study using fresh or predegenerated nerve grafts

Original Paper

Transient Axonal Injury in the Absence of Demyelination: A Correlate of Clinical Disease in Acute Experimental Autoimmune Encephalomyelitis

Original Paper

Canine cognitive deficit correlates with diffuse plaque maturation and S100β (−) astrocytosis but not with insulin cerebrospinal fluid level

Original Paper

Relative paucity of tau accumulation in the small areas with abundant Aβ42-positive capillary amyloid angiopathy within a given cortical region in the brain of patients with Alzheimer pathology