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DOI: 10.1055/s-2002-28469
Muscle Preservation by Prolonged Sensory Protection
Publication History
Publication Date:
13 May 2002 (online)
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ABSTRACT
The functional recovery of a muscle target following nerve repair is inversely related to the denervation time: i.e., the longer the muscle denervation, the poorer the functional outcome following nerve reconstruction. The trophic and protective effects of sensory innervation to a motor nerve, following prolonged denervation (greater than 6 months), have been studied. Following proximal transection of the musculocutaneous nerve (MC) close to its C6 origin in 10 adult male Sprague-Dawley rats, the severed nerve was coapted to supraclavicular purely sensory nerves originating from C3 and C4 (sensory protection [SP] group). In another 10 Sprague-Dawley rats, the transected MC nerve was not protected by coaptation to sensory nerves (control group). After prolonged denervation or ``sensory protection'' (6 months), the MC nerve was then coapted in both groups to the purely motor medial pectoral nerve. Behavioral testing (grooming test) was performed on a weekly basis during the reinnervation time, which lasted 4 weeks. Statistically significant differences (p<0.05) favoring the SP group, were found at the second week of the reinnervation period, but not at the end of the experiment. Evaluation also included intraoperative electrical stimulation of the MC nerve, biceps muscle dry weights, motor endplate counts, and nerve axon counts of the MC nerve. The biceps muscle dry weights were statistically higher in the SP group, along with a trend for a higher number of motor endplates. No statistically significant difference was found in the nerve axon counts of the MC nerve between the two groups. Statistically better intraoperative electrical stimulation results were also encountered in the sensory protection group. An interpretation of the results favors the hypothesis that sensory reinnervation of a motor target may provide the necessary trophic environment to minimize muscle atrophy, until a motor donor nerve becomes available.
KEYWORDS
Denervation - ``sensory protection,'' sensory reinnervation - motor target - minimizing muscle atrophy
REFERENCES
- 1 Fu S Y, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci . 1995; 15 3886-3895
- 2 Fu S Y, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J Neurosci . 1995; 15 3876-3885
- 3 Finkelstein D I, Dooley P C, Luff A R. Recovery of muscle after different periods of denervation and treatments. Muscle Nerve . 1993; 16 769-777
- 4 Ribaric S, Stefanovska A, Brzin M. Biochemical, morphological and functional changes during peripheral nerve regeneration. Mol Chem Neuropath . 1991; 15 143-157
- 5 Sunderland S. Changes in denervated muscle. In: Sunderland S, ed. Nerve Injuries and their Repair: A Critical Appraisal Edinburgh: Churchill-Livingston 1991: 241-247
- 6 Thanos P K, Terzis J K. Motor end plate analysis of the denervated and reinnervated orbicularis oculi muscle in the rat. J Reconstr Microsurg . 1995; 11 423-428
- 7 Virtanen P, Tolonen U, Savolainen J, Takala T. Effect of reinnervation on collagen synthesis in rat skeletal muscle. J Appl Physiol . 1992; 72 2069-2074
- 8 Love F M, Thompson W J. Schwann cells proliferate at rat neuromuscular junctions during development and regeneration. J Neurosci . 1998; 18 9376-9385
- 9 Hie N B, van Nie L C, Vermeulen-van der Zee E. Twitch tension, muscle weight and fiber area of exercised reinnervating rat skeletal muscle. Arch Phys Med Rehab . 1982; 63 608-612
- 10 Parry W CB, Frampton V, Monteith A. Rehabilitation of patients following traction lesions of the brachial plexus. In: Terzis JK, ed. Microreconstruction of Nerve Injuries Philadelphia, PA: WB Saunders Company 1987: 483-496
- 11 Kanaya F, Tajima T. Effect of electrostimulation on denervated muscle. Clin Orthop Rel Res . 1992; 283 296-301
- 12 Schimrigk K, McLaughlin J, Gruninger W. The effect of electrical stimulation on the experimentally denervated rat muscle. Scand J Rehab Med . 1977; 9 55-60
- 13 Schmalbruch H, Al-Amood W S, Lewis D M. Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J Physiol . 1991; 441 233-241
- 14 Liberson T W, Terzis J K. Contribution of clinical neurophysiology and rehabilitation medicine to the management of brachial plexus palsy. In: Terzis JK, ed. Microreconstruction of Nerve Injuries Philadelphia, PA: WB Saunders Company 1987: 555-566
- 15 Yin Q, Kemp G J, Frostick S P. Neurotrophins, neurons and peripheral nerve regeneration. J Hand Surg . 1998; 23B 433-437
- 16 Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J Anat . 1999; 194 1-14
- 17 Yamamori T, Fukada K, Aebershold R. The cholinergic neuronal differentiation factor from heart cells is identical to leukaemia inhibitory factor. Science . 1989; 246 1412-1416
- 18 Weiss P, Edds M. Sensory-motor nerve crosses in the rat. J Neurophysiol . 1945; 8 173-193
- 19 Gutmann E. The reinnervation of muscle by sensory nerve fibers. J Anat . 1945; 79 1-10
- 20 Zalewski A A. Effects of reinnervation on denervated skeletal muscle by axons of motor, sensory and sympathetic neurons. Am J Physiol . 1970; 219 1675-1679
- 21 Nishimura H, Johnson R D, Munson J B. Rescue of motorneurons from the axotomized state by regeneration into a sensory nerve in cats. J Neurophysiol . 1991; 66 1462-1470
- 22 Zhang F, Lineweaver W C, Ustuner T. Comparison of muscle mass preservation in denervated muscle and transplanted muscle flaps after motor and sensory reinnervation and neurotization. Plast Reconstr Surg . 1997; 99 803-814
- 23 Hynes N M, Bain J R, Thoma A. Preservation of denervated muscle by sensory protection in rats. J Reconstr Microsurg . 1997; 13 337-343
- 24 Bain J R, Veltri K L, Chamberlain D, Fahnestock M. Improved functional recovery of denervated skeletal muscle after temporary sensory nerve innervation. Neuroscience . 2001; 2 503-510
- 25 Wang H, Gu Y, Xu J. Comparative study of different surgical procedures using sensory nerves or neurons for delaying atrophy of denervated skeletal muscle. J Hand Surg . 2001; 26A 326-331
- 26 Ochi M, Kwong W H, Kimori K. Reinnervation of denervated skeletal muscles by grafted dorsal root ganglion. Exp Neurol . 1992; 118 291-301
- 27 Ochi M, Kwong W H, Kimori K. Delay of the denervation process in skeletal muscle by sensory ganglion graft and its clinical application. Plast Reconstr Surg . 1996; 97 577-586
- 28 Vera C L, Luco J V. Reinnervation of smooth and striated muscle by sensory nerves. J Neurophysiol . 1967; 30 620-628
- 29 Falempin M, Rousseeau J P. Reinnervation of skeletal muscles by vagal sensory fibers in the sheep, cat and rabbit. J Physiol . 1983; 335 467-479
- 30 Flumerfelt B A, Kiernan J P, Krcek J P, Sholdice J. Reinnervation of skeletal muscle in the tongue by preganglionic parasympathetic vagal neurons. J Anat . 1986; 146 117-130
- 31 Ebert D, Terzis J K. Denervated muscle preservation by sensory protection: a new animal model. Presented at: the 44th Annual Meeting of the Plastic Surgery Research Council; May 22-25 1999 Pittsburgh, PA
- 32 Carson K A, Terzis J K. Carbonic anhydrase histochemistry: a potential diagnostic method for peripheral nerve repair. Clin Plast Surg . 1985; 12 227-232
- 33 Inciong J GB, Marrocco W G, Terzis J K. Efficacy of intervention strategies in a brachial plexus global avulsion model in the rat. Plast Reconstr Surg . 2000; 105 2059-2071
- 34 Gorio A, Carmignoto G, Finesso M. Muscular reinnervation. II: Sprouting, synapse formation and repression. Neuroscience . 1983; 8 403-416
- 35 Kalantarian B, Rice D C, Tiangco D A, Terzis J K. Gains and losses of the XII-VII component of the ``baby-sitter'' procedure: a morphometric analysis. J Reconstr Microsurg . 1998; 14 459-471
- 36 Langley J N, Andersen H K. The union of different kinds of nerve fibers. J Physiol . 1904; 31 365-391
- 37 Elsberg C A. Experiments on motor nerve regeneration and direct neurotization of paralyzed muscles by their own and foreign nerves. Science . 1917; 45 318-320
- 38 Deckwerth T L, Johnson E M. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurones deprived of nerve growth factor. J Cell Biol . 1993; 123 1207-1222
- 39 James R, Tonra J R, Curtis R. Axotomy upregulates the anterograde transport and expression of brain derived neurotrophic factor in sensory neurons. J Neurosci . 1998; 18 4371-4383
- 40 Michael G J, Averill S, Nitkunan A. Nerve growth factor increases brain derived neurotrophic factor selectively in TrkA expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci . 1997; 17 8476-8490
- 41 Lewin S L, Utley D S, Chenget K. Simultaneous treatment with BDNF and CNTF after peripheral nerve transection and repair enhances rate of functional recovery compared with BDNF treatment alone. Laryngoscope . 1997; 107 992-999