Basic Science of Muscle Neurotization: A Review

Abstract

Traumatic nerve injuries continue to be considered a challenge in the field of nerve microsurgical reconstruction. Despite the advances in microsurgical repair techniques, motor function recovery is not adequate in severe nerve injuries, especially when there is separation of the motor nerve from the muscle tissue. The technique of reinnervating skeletal muscles by insertion within it of a donor nerve was developed at the beginning of the 20th century during World War I, when injuries and poliomyelitis produced paralytics for whom no therapy was available. Only a few reports of clinically successful reinnervation exist, and clinical application of the method during the following decades has been limited. However, the functional value of this procedure remains a matter of controversy. The purpose of this review is to present what is known in basic science about direct neurotization of muscle along with a brief historical review.

Keywords

direct neurotization of muscle - muscle denervation - nerve repair - nerve regeneration

• References

• 1 Swanson AN, Wolfe SW, Khazzam M, Feinberg J, Ehteshami J, Doty S. Comparison of neurotization versus nerve repair in an animal model of chronically denervated muscle. J Hand Surg Am 2008; 33 (7) 1093-1099
• 2 Meals RA, Nelissen RG. The origin and meaning of “neurotization”. J Hand Surg Am 1995; 20 (1) 144-146
• 3 Hacker V. Erfolgreich operativ behandelte cucullarislahmung. Wien Klin Wehnschr 1908; 21 (2) 1314
• 4 Sorbie C, Porter TL. Reinnervation of paralysed muscles by direct motor nerve implantation. An experimental study in the dog. J Bone Joint Surg Br 1969; 51 (1) 156-164
• 5 Park DM, Shon SK, Kim YJ. Direct muscle neurotization in rat soleus muscle. J Reconstr Microsurg 2000; 16 (5) 379-383
• 6 Askar I, Sabuncuoglu BT, Yormuk E, Saray A. The fate of neurotization techniques on reinnervation after denervation of the gastrocnemius muscle: an experimental study. J Reconstr Microsurg 2001; 17 (5) 347-355 , discussion 355–356
• 7 Dy CJ, Kitay A, Garg R, Kang L, Feinberg JH, Wolfe SW. Neurotization to innervate the deltoid and biceps: 3 cases. J Hand Surg Am 2013; 38 (2) 237-240
• 8 Heineke H. Die direkte Einpflanzung der Nerven in den Muskel. Zentralbl Chir 1914; 41: 465-466
• 9 Steindler A. The method of direct neurotization of paralyzed muscles. Am J Orthop Surg 1915; 13: 33-45
• 10 Erlacher P. Direct and muscular neurotization of paralyzed muscles. Am J Orthop Surg 1915; 13: 22-32
• 11 Aitken JT. Growth of nerve implants in voluntary muscle. J Anat 1950; 84 (Pt 1) 38-49
• 12 Sakellarides HT, Sorbie C, James L. Reinnervation of denervated muscles by nerve transplantation. Clin Orthop Relat Res 1972; 83 (83) 195-201
• 13 Brunelli G, Monini L, Antonucci A , et al. Neurotizzazione in zona aneurale di muscoli denervati. Policlinico 1976; 83: 611-616
• 14 Brunelli GA, Brunelli GR. Direct muscle neurotization. J Reconstr Microsurg 1993; 9 (2) 81-90 , discussion 89–90
• 15 Payne Jr SH, Brushart TM. Neurotization of the rat soleus muscle: a quantitative analysis of reinnervation. J Hand Surg Am 1997; 22 (4) 640-643
• 16 Millesi H. Peripheral nerve repair: terminology, questions, and facts. J Reconstr Microsurg 1985; 2 (1) 21-31
• 17 Francel TJ, Dellon AL. Functional limb salvage combining gastrocnemius neurotization and posterior tibial nerve grafting: a case report. J Reconstr Microsurg 1992; 8 (3) 209-213 , discussion 213–214
• 18 Mackinnon SE, McLean JA, Hunter GA. Direct muscle neurotization recovers gastrocnemius muscle function. J Reconstr Microsurg 1993; 9 (2) 77-80
• 19 Brunelli GA. Direct Muscular Neurotization. J Am Soc Surg Hand 2005; 5 (4) 193-200
• 20 Becker M, Lassner F, Fansa H, Mawrin C, Pallua N. Refinements in nerve to muscle neurotization. Muscle Nerve 2002; 26 (3) 362-366
• 21 Guth L, Zalewski AA. Disposition of cholinesterase following implantation of nerve into innervated and denervated muscle. Exp Neurol 1963; 7: 316-326
• 22 Frey M, Gruber H, Holle J, Freilinger G. An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization. Plast Reconstr Surg 1982; 69 (4) 656-669
• 23 Brunelli G, Brunelli LM. Direct neurotization of severely damaged denervated muscles. Int Surg 1980; 65 (6) 529-531
• 24 Kumai Y, Ito T, Matsukawa A, Yumoto E. Effects of denervation on neuromuscular junctions in the thyroarytenoid muscle. Laryngoscope 2005; 115 (10) 1869-1872
• 25 Sunderland S. Morphological changes in striated muscle due to denervation. Atrophy. In: Sunderland S, , ed. Nerves and Nerve Injuries. Melbourne: Williams and Wilkins; 1968
• 26 Carlson BM, Billington L, Faulkner J. Studies on the regenerative recovery of long-term denervated muscle in rats. Restor Neurol Neurosci 1996; 10 (2) 77-84
• 27 Frank E, Gautvik K, Sommerschild H. Persistence of junctional acetylcholine receptors following denervation. Cold Spring Harb Symp Quant Biol 1976; 40: 275-281
• 28 Salpeter MM, Loring RH. Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Prog Neurobiol 1985; 25 (4) 297-325
• 29 Witzemann V, Brenner HR, Sakmann B. Neural factors regulate AChR subunit mRNAs at rat neuromuscular synapses. J Cell Biol 1991; 114 (1) 125-141
• 30 Brunelli G, Monini L. Direct muscular neurotization. J Hand Surg Am 1985; 10 (6, Pt 2) 993-997
• 31 Gwyn DG, Aitken JT. The formation of new motor endplates in mammalian skeletal muscle. J Anat 1966; 100 (Pt 1) 111-126
• 32 Rice DH, Owens O, Burstein F, Verity A. The nerve-muscle pedicle. A visual, electromyographic, and histochemical study. Arch Otolaryngol 1983; 109 (4) 233-234
• 33 Rubin LL, Schuetze SM, Weill CL, Fischbach GD. Regulation of acetylcholinesterase appearance at neuromuscular junctions in vitro. Nature 1980; 283 (5744) 264-267
• 34 Warszawski M, Telerman-Toppet N, Durdu J, Graff GL, Coërs C. The early stages of neuromuscular regeneration after crushing the sciatic nerve in the rat. Electrophysiological and histological study. J Neurol Sci 1975; 24 (1) 21-32
• 35 Gray WP, Keohane C, Kirwan WO. Motor nerve transplantation. J Neurosurg 1997; 87 (4) 615-624
• 36 Chen LE, Seaber AV, Urbaniak JR, Murrell GA. Denatured muscle as a nerve conduit: a functional, morphologic, and electrophysiologic evaluation. J Reconstr Microsurg 1994; 10 (3) 137-144
• 37 Kim PS, Ko JH, O'Shaughnessy KK, Kuiken TA, Pohlmeyer EA, Dumanian GA. The effects of targeted muscle reinnervation on neuromas in a rabbit rectus abdominis flap model. J Hand Surg Am 2012; 37 (8) 1609-1616
• 38 Gutmann E. Denervation and disuse atrophy in crosstriated muscle. Rev Can Biol 1962; 21: 353-365
• 39 Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci 1995; 15 (5, Pt 2) 3886-3895
• 40 Keilhoff G, Fansa H. Successful intramuscular neurotization is dependent on the denervation period. A histomorphological study of the gracilis muscle in rats. Muscle Nerve 2005; 31 (2) 221-228
• 41 Terzis JK, Karypidis D. Outcomes of direct muscle neurotization in pediatric patients with facial paralysis. Plast Reconstr Surg 2009; 124 (5) 1486-1498
• 42 Verdú E, Ceballos D, Vilches JJ, Navarro X. Influence of aging on peripheral nerve function and regeneration. J Peripher Nerv Syst 2000; 5 (4) 191-208
• 43 Kawabuchi M, Zhou CJ, Wang S, Nakamura K, Liu WT, Hirata K. The spatiotemporal relationship among Schwann cells, axons and postsynaptic acetylcholine receptor regions during muscle reinnervation in aged rats. Anat Rec 2001; 264 (2) 183-202
• 44 Deschenes MR, Wilson MH. Age-related differences in synaptic plasticity following muscle unloading. J Neurobiol 2003; 57 (3) 246-256
• 45 Wang YJ, Zhou CJ, Shi Q, Smith N, Li TF. Aging delays the regeneration process following sciatic nerve injury in rats. J Neurotrauma 2007; 24 (5) 885-894
• 46 Apel PJ, Alton T, Northam C , et al. How age impairs the response of the neuromuscular junction to nerve transection and repair: an experimental study in rats. J Orthop Res 2009; 27 (3) 385-393
• 47 Terzis JK, Konofaos P. Nerve transfers in facial palsy. Facial Plast Surg 2008; 24 (2) 177-193
• 48 Bertelli JA, Taleb M, Mira JC, Ghizoni MF. Variation in nerve autograft length increases fibre misdirection and decreases pruning effectiveness: an experimental study in the rat median nerve. Neurol Res 2005; 27 (6) 657-665
• 49 Noordin S, Ahmed M, Rehman R, Ahmad T, Hashmi P. Neuronal regeneration in denervated muscle following sensory and muscular neurotization. Acta Orthop 2008; 79 (1) 126-133
• 50 Tews DS, Goebel HH, Schneider I, Gunkel A, Stennert E, Neiss WF. Morphology of experimentally denervated and reinnervated rat facial muscle. I. Histochemical and histological findings. Eur Arch Otorhinolaryngol 1994; 251 (1) 36-40
• 51 Menderes A, Yilmaz M, Vayvada H, Ozer E, Barutçu A. Effects of nerve growth factor on the neurotization of denervated muscles. Ann Plast Surg 2002; 48 (4) 415-422