Transection of peripheral nerves, bridging strategies and effect evaluation.

Disruption of peripheral nerves due to trauma is a frequently occurring clinical problem. Gaps in the nerve are bridged by guiding the regenerating nerves along autologous grafts or artificial guides. This review gives an overview on the different methods of nerve repair techniques. Conventional suturing techniques are discussed as well as the use of e.g. biological, synthetic, non-degradable or degradable nerve guides. Functional assessment showed that repair of a gap with a bio-degradable guide is superior to that with autologous grafts. But still, long lasting changes were observed in the Sciatic Function Index (SFI), abnormal walking patterns, disturbed Electro Myo Graphic (EMG) patterns, next to shifts in the histochemical properties of the muscles and longlasting abnormalities in neuromuscular contacts. These phenomena are explained by an at-random reinnervation. When transecting the nerve at young ages, this did not lead to enhanced recovery. Rearing rats operated at adult age in an enriched environment, also had no beneficial effect. Future research should aim at developing longer guides, possibly lined with Schwann cells, or additives, improving specific reinnervation of the former target areas.

[1]  R. Melzack,et al.  Deafferentation and chronic pain in animais: An evaluation of evidence suggesting autotomy is related to pain , 1986, Pain.

[2]  M. Wiberg,et al.  Poly-3-hydroxybutyrate (PHB): a resorbable conduit for long-gap repair in peripheral nerves. , 2002, British journal of plastic surgery.

[3]  D. N. Landon Peripheral Nerve , 2020, Congress of Neurological Surgeons Essent.

[4]  L A van Eykern,et al.  A new technique for simultaneously recording EMG and movements in experimental animals. , 2001, Brain research. Brain research protocols.

[5]  Christine K. Thomas,et al.  Muscle Reinnervation with Delayed or Immediate Transplant of Embryonic Ventral Spinal Cord Cells into Adult Rat Peripheral Nerve , 2002, Cell transplantation.

[6]  C. Krarup,et al.  Factors that influence peripheral nerve regeneration: An electrophysiological study of the monkey median nerve , 2002, Annals of neurology.

[7]  B. Uzman,et al.  Mouse sciatic nerve regeneration through semipermeable tubes: A quantitative model , 1983, Journal of neuroscience research.

[8]  Josef Donnerer,et al.  Regeneration of Primary Sensory Neurons , 2003, Pharmacology.

[9]  Jian Zhang,et al.  Autogenous venous graft with one-stage prepared Schwann cells as a conduit for repair of long segmental nerve defects. , 2002, Journal of reconstructive microsurgery.

[10]  W. Freed,et al.  An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks , 1982, Experimental Neurology.

[11]  C. Krarup,et al.  Early peripheral nerve regeneration after crushing, sectioning, and freeze studied by implanted electrodes in the cat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Abraham Zangen,et al.  Correlation of intact sensibility and neuropathic pain-related behaviors in eight inbred and outbred rat strains and selection lines , 2001, Pain.

[13]  P H Robinson,et al.  Electronmicroscopical evaluation of short-term nerve regeneration through a thin-walled biodegradable poly(DLLA-epsilon-CL) nerve guide filled with modified denatured muscle tissue. , 2001, Biomaterials.

[14]  D. Grijpma,et al.  In vivo and in vitro degradation of poly[50/50 (85/15L/D)LA/ε-CL], and the implications for the use in nerve reconstruction , 2000 .

[15]  P H Robinson,et al.  Long‐term evaluation of functional nerve recovery after reconstruction with a thin‐walled biodegradable poly (DL‐Lactide‐ϵ‐caprolactone) nerve guide, using walking track analysis and electrostimulation tests , 1999, Microsurgery.

[16]  S. McMahon,et al.  Neurotrophin-3-Mediated Regeneration and Recovery of Proprioception Following Dorsal Rhizotomy , 2002, Molecular and Cellular Neuroscience.

[17]  R. Stein,et al.  Time course and extent of recovery in reinnervated motor units of cat triceps surae muscles , 1982, The Journal of physiology.

[18]  G. Beer,et al.  The toe-spreading reflex of the rabbit revisited-functional evaluation of complete peroneal nerve lesions , 2001, Laboratory animals.

[19]  M. Meek,et al.  Peripheral Nerve Regeneration and Functional Nerve Recovery After Reconstruction with a Thin-Walled Biodegradable Poly(DL-lactide-ε-caprolactone) Nerve Guide , 1997 .

[20]  P. Klopper,et al.  Vein graft conduits versus conventional suturing in peripheral nerve reconstructions , 1993, Microsurgery.

[21]  M. Akagi,et al.  Bridging a peripheral nerve defect using collagen filaments. , 2001, The Journal of hand surgery.

[22]  T. Gordon,et al.  Comparison of injury and development in the neuromuscular system. , 1988, Ciba Foundation symposium.

[23]  F. Gage,et al.  Neural consequences of enviromental enrichment , 2000, Nature Reviews Neuroscience.

[24]  K. Tark,et al.  Morphometric study of regeneration through vascularized nerve graft in a rabbit sciatic nerve model. , 2001, Journal of reconstructive microsurgery.

[25]  James N. Campbell,et al.  Complications from silicon‐polymer intubulation of nerves , 1989, Microsurgery.

[26]  P H Robinson,et al.  Nerve regeneration through a two‐ply biodegradable nerve guide in the rat and the influence of ACTH4‐9 nerve growth factor , 1991, Microsurgery.

[27]  D. Bryan,et al.  Effect of Schwann Cells in the Enhancement of Peripheral-Nerve Regeneration , 1996, Journal of reconstructive microsurgery.

[28]  J. Swett,et al.  Motor versus Sensory Neuron Regeneration through Collagen Tubules , 1998, Plastic and reconstructive surgery.

[29]  G. O'Hanlon,et al.  Nerve injury in adult rats causes abnormalities in the motoneuron dendritic field that differ from those seen following neonatal nerve injury , 2004, Experimental Brain Research.

[30]  M. Wasserschaff Coordination of reinnervated muscle and reorganization of spinal cord motoneurons after nerve transection in mice , 1990, Brain Research.

[31]  S. Lipton,et al.  Acidic Fibroblast Growth Factor Enhances Peripheral Nerve Regeneration in Vivo , 1989, Plastic and reconstructive surgery.

[32]  F. Plum Handbook of Physiology. , 1960 .

[33]  J. Lewin-Kowalik,et al.  Pre-degenerated peripheral nerve extracts applied to the proximal stump of transected sciatic nerve enhance both regeneration and autotomic behavior in rats. , 2002, Medical science monitor : international medical journal of experimental and clinical research.

[34]  T. Kauppila Correlation between autotomy-behavior and current theories of neuropathic pain , 1998, Neuroscience & Biobehavioral Reviews.

[35]  R. Burke Motor Units: Anatomy, Physiology, and Functional Organization , 1981 .

[36]  J. Eccles,et al.  Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses , 1960, The Journal of physiology.

[37]  J B Tang,et al.  Vein conduits for repair of nerves with a prolonged gap or in unfavorable conditions: An analysis of three failed cases , 1995, Microsurgery.

[38]  T. van Laar,et al.  Effects of enriched housing on functional recovery after spinal cord contusive injury in the adult rat. , 2001, Journal of neurotrauma.

[39]  A. Gramsbergen,et al.  Transection of the sciatic nerve and reinnervation in adult rats: muscle and endplate morphology. , 2001, Equine veterinary journal. Supplement.

[40]  R. Ribchester Development and plasticity of neuromuscular innervation , 2005 .

[41]  B. Seckel,et al.  Hyaluronic acid through a new injectable nerve guide delivery system enhances peripheral nerve regeneration in the rat , 1995, Journal of neuroscience research.

[42]  R. Shi,et al.  Polyethylene Glycol Rapidly Restores Physiological Functions in Damaged Sciatic Nerves of Guinea Pigs , 2002, Neurosurgery.

[43]  Tatsuo Nakamura,et al.  Use of a Newly Developed Artificial Nerve Conduit to Assist Peripheral Nerve Regeneration Across a Long Gap in Dogs , 2000, ASAIO journal.

[44]  Xavier Navarro,et al.  Bimodal dose‐dependence of FK506 on the rate of axonal regeneration in mouse peripheral nerve , 2002, Muscle & nerve.

[45]  M. Meek,et al.  Clinical Use of Nerve Conduits in Peripheral-Nerve Repair: Review of the Literature , 2002, Journal of reconstructive microsurgery.

[46]  J. G. van Dijk,et al.  Obstetric lesions of the brachial plexus , 2001, Muscle & nerve.

[47]  P H Robinson,et al.  [A degradable artificial nerve guide to bridge peripheral nerve defects]. , 2003, Nederlands tijdschrift voor geneeskunde.

[48]  Taylor Gi,et al.  The free vascularized nerve graft. A further experimental and clinical application of microvascular techniques. , 1976 .

[49]  W. Partata,et al.  Sciatic nerve transection decrease substance P immunoreactivity in the lumbosacral spinal cord of the frog (Rana catesbeiana). , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[50]  A. J. Harris,et al.  Accuracy in peripheral nerve regeneration , 1981, Trends in Neurosciences.

[51]  J. Bertelli,et al.  The rat brachial plexus and its terminal branches: An experimental model for the study of peripheral nerve regeneration , 1995, Microsurgery.

[52]  G. Lundborg,et al.  Ulnar nerve repair by the silicone chamber technique. Case report. , 1991, Scandinavian journal of plastic and reconstructive surgery and hand surgery.

[53]  B. Seckel,et al.  Inside‐outl vein graft repair compared with nerve grafting for nerve regeneration in rats , 1995, Microsurgery.

[54]  D Schonfeld,et al.  Two modes of cutaneous reinnervation following peripheral nerve injury , 1979, The Journal of comparative neurology.

[55]  TM Brushart,et al.  Preferential reinnervation of motor nerves by regenerating motor axons , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  H. Romijn,et al.  At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? , 1991, Early human development.

[57]  E Stennert,et al.  Slow Axonal Regrowth But Extreme Hyperinnervation of Target Muscle After Suture of the Facial Nerve in Aged Rats , 1998, Neurobiology of Aging.

[58]  J. Larosse,et al.  Autologous Denatured Muscle as a Nerve Graft , 1994, Journal of reconstructive microsurgery.

[59]  Bora Fw Peripheral nerve repair in cats. The fascicular stitch. , 1967 .

[60]  T Gordon,et al.  Brief Electrical Stimulation Promotes the Speed and Accuracy of Motor Axonal Regeneration , 2000, The Journal of Neuroscience.

[61]  A. Gentile,et al.  Enrichment versus exercise effects on motor impairments following cortical removals in rats. , 1987, Behavioral and neural biology.

[62]  S. Kennedy,et al.  Quantitative aspects of normal locomotion in rats. , 1979, Life sciences.

[63]  P. Murphy,et al.  Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. , 1986, The Journal of physiology.

[64]  D. Green,et al.  Operative hand surgery , 1983 .

[65]  The Current Status of Peripheral Nerve Regeneration , 1990 .

[66]  J. Terzis Microreconstruction of Nerve Injuries , 1987 .

[67]  Göran Lundborg,et al.  Nerve Injury and Repair , 1988 .

[68]  S. Kay,et al.  Obstetrical brachial palsy. , 1998, British journal of plastic surgery.

[69]  D. H. Kim,et al.  Comparison of macropore, semipermeable, and nonpermeable collagen conduits in nerve repair. , 1993, Journal of reconstructive microsurgery.

[70]  P. Helders,et al.  Exercise training improves functional recovery and motor nerve conduction velocity after sciatic nerve crush lesion in the rat. , 1997, Archives of physical medicine and rehabilitation.

[71]  D. Clemente,et al.  Effects of axotomy on the expression of NADPH-diaphorase in the visual pathway of the tench , 2002, Brain Research.

[72]  M. Zimmermann,et al.  Pathobiology of neuropathic pain. , 2001, European journal of pharmacology.

[73]  P H Robinson,et al.  Two-ply biodegradable nerve guide: basic aspects of design, construction and biological performance. , 1990, Biomaterials.

[74]  G. Lundborg,et al.  Can Sensory and Motor Collateral Sprouting be Induced from Intact Peripheral Nerve by End-to-Side Anastomosis? , 1994, Journal of hand surgery.

[75]  J. R. Hoffman,et al.  Nerve growth factor and neurotrophin-3 affect functional recovery following peripheral nerve injury differently. , 2001, Restorative neurology and neuroscience.

[76]  Keiko Okamoto,et al.  Extracellular matrix of human amnion manufactured into tubes as conduits for peripheral nerve regeneration. , 2002, Journal of biomedical materials research.

[77]  S. Mackinnon,et al.  Wire mesh as a post-operative physiotherapy assistive device following peripheral nerve graft repair in the rat. , 1996, Journal of the peripheral nervous system : JPNS.

[78]  A. Berger,et al.  The Interfascicular Nerve-grafting of the Median and Ulnar Nerves , 1972 .

[79]  M. Meek,et al.  Evaluation of Functional Nerve Recovery after Reconstruction with a New Biodegradable Poly (DL-Lactide-∊-Caprolactone) Nerve Guide , 1997, The International journal of artificial organs.

[80]  P H Robinson,et al.  Evaluation of functional nerve recovery after reconstruction with a poly (DL‐Lactide‐ϵ‐Caprolactone) nerve guide, filled with modified denatured muscle tissue , 1996, Microsurgery.

[81]  G. Murrell,et al.  Denatured Muscle as a Nerve Conduit: A Functional, Morphologic, and Electrophysiologic Evaluation , 1994, Journal of reconstructive microsurgery.

[82]  A. Gramsbergen,et al.  Sciatic Nerve Transection in the Adult Rat: Abnormal EMG Patterns during Locomotion by Aberrant Innervation of Hindleg Muscles , 2000, Experimental Neurology.

[83]  M. Meek,et al.  Sensory nerve function and auto-mutilation after reconstruction of various gap lengths with nerve guides and autologous nerve grafts. , 2001, Biomaterials.

[84]  J. Rosen,et al.  The Artificial Nerve Graft: A Comparison of Blended Elastomer-Hydrogel with Polyglycolic Acid Conduits , 1991, Journal of reconstructive microsurgery.

[85]  A. Gramsbergen,et al.  Muscle differentiation after sciatic nerve transection and reinnervation in adult rats. , 2001, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[86]  W. Gispen,et al.  Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  P. Murphy,et al.  Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation. , 1987, Journal of neurophysiology.

[88]  Tessa Gordon,et al.  Electrical Stimulation Promotes Motoneuron Regeneration without Increasing Its Speed or Conditioning the Neuron , 2002, The Journal of Neuroscience.

[89]  A. Gramsbergen,et al.  Polyneural innervation in the psoas muscle of the developing rat , 1998, Muscle & nerve.

[90]  M Moras,et al.  Biocompatibility and biodegradation of different hyaluronan derivatives (Hyaff) implanted in rats. , 1993, Biomaterials.

[91]  M. Meek,et al.  Functional evaluation of peripheral nerve regeneration in the rat: walking track analysis , 2001, Journal of Neuroscience Methods.

[92]  G. Weddell,et al.  THE LOCAL EXTENSION OF NERVE FIBRES INTO DENERVATED AREAS OF SKIN , 1941 .

[93]  S. BeMent,et al.  Comparison of methods of peripheral nerve suturing in monkeys. , 1970, Plastic and reconstructive surgery.

[94]  A Gramsbergen,et al.  Handbook of Brain and Behaviour in Human Development. , 2001 .

[95]  TM Brushart,et al.  Motor axons preferentially reinnervate motor pathways , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[96]  S. Mackinnon,et al.  Functional Evaluation of Complete Sciatic, Peroneal, and Posterior Tibial Nerve Lesions in the Rat , 1989, Plastic and reconstructive surgery.

[97]  H. Iizuka,et al.  Developmental alteration of nerve injury induced glial cell line‐derived neurotrophic factor (GDNF) receptor expression is crucial for the determination of injured motoneuron fate , 2002, Journal of neurochemistry.

[98]  W. Gispen,et al.  Methods for producing a reproducible crush in the sciatic and tibial nerve of the rat and rapid and precise testing of return of sensory function Beneficial effects of melanocortins , 1986, Journal of the Neurological Sciences.

[99]  Comtet Jj [Vascularized nerve grafts]. , 1983, Acta chirurgica Belgica.

[100]  B Battiston,et al.  Nerve repair by means of vein filled with muscle grafts. II. Morphological analysis of regeneration , 2000, Microsurgery.

[101]  EXPERIMENTAL PERIPHERAL NERVE REPAIR TUBULATION. , 1964 .

[102]  H. Millesi The current state of peripheral nerve surgery in the upper limb. , 1984, Annales de chirurgie de la main : organe officiel des societes de chirurgie de la main.

[103]  C. Govind,et al.  Remodeling of the proximal segment of crayfish motor nerves following transection , 2002, The Journal of comparative neurology.

[104]  M. Ebelin,et al.  Résultats de la réparation primaire de vingt-huit plaies isolées du nerf médian au poignet , 1989 .

[105]  Albert Gramsbergen,et al.  Methods to evaluate functional nerve recovery in adult rats: walking track analysis, video analysis and the withdrawal reflex , 2000, Journal of Neuroscience Methods.

[106]  J. Holle,et al.  An Experimental Comparison of the Different Kinds of Muscle Reinnervation: Nerve Suture, Nerve Implantation, and Muscular Neurotization , 1982, Plastic and reconstructive surgery.

[107]  Xavier Navarro,et al.  H reflex restitution and facilitation after different types of peripheral nerve injury and repair , 2001, Brain Research.

[108]  A. Gramsbergen,et al.  Sciatic nerve transection in adult and young rats: abnormal EMG patterns during locomotion. , 2001, Equine veterinary journal. Supplement.

[109]  M. Yamashiro,et al.  Effectiveness of Cervical Sympathetic Ganglia Block on Regeneration of the Trigeminal Nerve Following Transection in Rats , 2001, Regional Anesthesia & Pain Medicine.

[110]  M. Botte,et al.  Inaccurate projection of rat soleus motoneurons: A comparison of nerve repair techniques , 1997, Muscle & nerve.

[111]  A. Gramsbergen,et al.  Functional assessment of sciatic nerve reconstruction: Biodegradable poly (DLLA‐ϵ‐CL) nerve guides versus autologous nerve grafts , 1999, Microsurgery.

[112]  R. Braun Epineurial nerve suture. , 1982, Clinical orthopaedics and related research.

[113]  S. Mackinnon,et al.  Chronic Nerve Compression—an Experimental Model in the Rat , 1984, Annals of plastic surgery.

[114]  D. Troost,et al.  Hyperthermic injury versus crush injury in the rat sciatic nerve: A comparative functional, histopathological and morphometrical study , 1992, Journal of the Neurological Sciences.

[115]  T. Gordon,et al.  Incomplete rematching of nerve and muscle properties in motor units after extensive nerve injuries in cat hindlimb muscle , 1998, The Journal of physiology.

[116]  A Gramsbergen,et al.  Biodegradable p(DLLA‐ϵ‐CL) nerve guides versus autologous nerve grafts: Electromyographic and video analysis , 2001, Muscle & nerve.

[117]  P. Mailänder,et al.  Advances in peripheral nerve repair in emergency surgery of the hand , 1991, World Journal of Surgery.

[118]  J. Terzis,et al.  Vascularized Nerve Grafts: An Experimental and Clinical Review , 1987, Annals of plastic surgery.

[119]  M. Godschalk,et al.  A magnetic evaluation of peripheral nerve regeneration: II. The signal amplitude in the distal segment in relation to functional recovery , 1998, Muscle & nerve.

[120]  D. F. Davey,et al.  Peripheral nerve regeneration through nerve guides seeded with adult Schwann cells , 1997, Neuropathology and applied neurobiology.

[121]  Joyce Evans,et al.  Gait-stance duration as a measure of injury and recovery in the rat sciatic nerve model , 1994, Journal of Neuroscience Methods.

[122]  G. Vrbóva,et al.  Axotomized Motoneurons Can Be Rescued from Cell Death by Peripheral Nerve Grafts: The Effect of Donor Age , 2003, Journal of neuropathology and experimental neurology.

[123]  J. Schröder,et al.  Abnormal sensory and motor reinnervation of rat muscle spindles following nerve transection and suture , 2004, Acta Neuropathologica.