Repair of Partial Lesions with Nerve Grafting Methods in the Rat Tibial Nerve

ABSTRACT

A partial nerve lesion and associated neuroma can be either left alone or repaired with a graft. A by-pass graft around the undisturbed lesion with end-to-side attachments might be a good alternative. This study in rats examines these strategies using walking-track analysis, muscle weights, and histology. After a tibial nerve partial lesion (3 mm) and a 21-day delay, the reexposed lesion was either not repaired, repaired with an interposed allograft, or a by-pass allograft. Functional results showed that all three groups had a steady improvement over the 8-week period, but without significant group differences. Gastrocnemius muscle ratios reflected intermediate atrophy. Axons regenerating through the lesion were more advanced than those which regenerated through the grafts and a neuroma was absent. The partial lesion can regenerate to an intermediate level without any intervention, including a by-pass graft, although the delayed repair strategy may have counteracted any potential benefits.

End-to-side - partial nerve lesion - nerve grafting - walking track analysis

REFERENCES

• 1 Hurst L C, Dowd A. Partial nerve injuries. In: Gelberman RH Operative Nerve Repair and Reconstruction New York; J.B. Lippincott Company 1991: 335-345
• 2 Midha R, Kline D G. Evaluation of the neuroma in continuity. In: Omer Jr GE, Spinner M, Van Beek AL Management of Peripheral Nerve Problems Philadelphia; Saunders 1997: 319-327
• 3 Sunderland S. Consequences of Disruption of the Endoneurium and Perineurium. Neuroma Formation. Fibre Interaction and the Artificial Synapse. Nerves and Nerve Injuries Baltimore, MD; Williams and Wilkins Company 1968: 180-193
• 4 Kline D G, Nulsen F E. The neuroma in continuity. Its preoperative and operative management.  Surg Clin North Am. 1972;  52 1189-1209
• 5 Vernadakis A J, Koch H, Mackinnon S E. Management of neuromas.  Clin Plast Surg. 2003;  30 247-268
• 6 Balance C A, Balance H A, Stewart P. Remarks on the operative treatment of chronic facial palsy of peripheral origin.  Br J Med. 1903;  2 1009-1013
• 7 Viterbo F, Trindade J C, Hoshino K, Mazzoni N A. End-to-side neurorrhaphy with removal of the epineurial sheath: an experimental study in rats.  Plast Reconstr Surg. 1994;  94 1038-1047
• 8 Lundborg G, Zhao Q, Kanje M, Danielsen N, Kerns J M. Can sensory and motor collateral sprouting be induced from intact peripheral nerve by end-to-side anastomosis?.  J Hand Surg. 1994;  19B 277-282
• 9 Aszmann O C, Korak K J, Rab M, Grunbeck M, Lassmann H, Frey M. Neuroma prevention by end-to-side neurorraphy: an experimental study in rats.  J Hand Surg. 2003;  28A 1022-1028
• 10 Kasabian A, Karp N, Margiotta M. Treatment of a neuroma-in-continuity of the peroneal nerve with nerve bypass grafts-a case report.  Ann Plast Surg. 1999;  42 449-451
• 11 Low C K, Chew S H, Song I C, Ng T H, Low Y P. End-to-side anastomosis of transected nerves to prevent neuroma formation.  Clin Orthop. 1999;  327-332
• 12 Shah M H, Kasabian A K, Karp N S et al.. Axonal regeneration through an autogenous nerve bypass: an experimental study in the rat.  Ann Plast Surg. 1997;  38 408-414
• 13 Zhang F, Fischer K A. End-to-side neurorrhaphy.  Microsurgery. 2002;  22 122-127
• 14 McCallister W V, Cober S R, Norman A, Trumble T E. Using intact nerve to bridge peripheral nerve defects: an alternative to the use of nerve grafts.  J Hand Surg. 2001;  26A 315-325
• 15 Bertelli J A, Dos Santos A R, Calixto J B. Is axonal sprouting able to traverse the conjunctival layers of the peripheral nerve? A behavioral, motor, and sensory study of end-to-side nerve anastomosis.  J Reconstr Microsurg. 1996;  12 559-563
• 16 De Sa J M, Mazzer N, Barbieri C H, Barreira A A. The end-to-side peripheral nerve repair: functional and morphometric study using the peroneal nerve of rats.  J Neurosci Methods. 2004;  136 45-53
• 17 Giovanoli P, Koller R, Meuli-Simmen C et al.. Functional and morphometric evaluation of end-to-side neurorrhaphy for muscle reinnervation.  Plast Reconstr Surg. 2000;  106 383-392
• 18 Kovacic U, Bajrovic F, Sketelj J. Recovery of cutaneous pain sensitivity after end-to-side nerve repair in the rat.  J Neurosurg. 1999;  91 857-862
• 19 Tarasidis G, Watanabe O, Mackinnon S E, Strasberg S R, Haughey B H, Hunter D A. End-to-side neurorrhaphy: a long-term study of neural regeneration in a rat model.  Otolaryngol Head Neck Surg. 1998;  119 337-341
• 20 Goheen-Robillard B, Myckatyn T M, Mackinnon S E, Hunter D A. End-to-side neurorrhaphy and lateral axonal sprouting in a long graft rat model.  Laryngoscope. 2002;  112 899-905
• 21 Rovak J M, Cederna P S, Macionis V, Urbanchek M S, Van Der Meulen J H, Kuzon Jr W M. Termino-lateral neurorrhaphy: the functional axonal anatomy.  Microsurgery. 2000;  20 6-14
• 22 Tham S K, Morrison W A. Motor collateral sprouting through an end-to-side nerve repair.  J Hand Surg. 1998;  23A 844-851
• 23 Okajima S, Terzis J K. Ultrastructure of early axonal regeneration in an end-to-side neurorrhaphy model.  J Reconstr Microsurg. 2000;  16 313-323
• 24 Noah E M, Williams A, Fortes W, Terzis J K. A new animal model to investigate axonal sprouting after end-to-side neurorrhaphy.  J Reconstr Microsurg. 1997;  13 317-325
• 25 al Qattan M M, al Thunyan A. Variables affecting axonal regeneration following end-to-side neurorrhaphy.  Br J Plast Surg. 1998;  51 238-242
• 26 Liu K, Chen L E, Seaber A V, Goldner R V, Urbaniak J R. Motor functional and morphological findings following end-to-side neurorrhaphy in the rat model.  J Orthop Res. 1999;  17 293-300
• 27 Kerns J M, Braverman B, Mathew A, Lucchinetti C, Ivankovich A D. A comparison of cryoprobe and crush lesions in the rat sciatic nerve.  Pain. 1991;  47 31-39
• 28 Kerns J M, Lucchinetti C. Electrical field effects on crushed nerve regeneration.  Exp Neurol. 1992;  117 71-80
• 29 Sobeski J K, Kerns J M, Safanda J F, Shott S, Gonzalez M H. Functional and structural effects of GM-1 ganglioside treatment on peripheral nerve grafting in the rat.  Microsurgery. 2001;  21 108-115
• 30 de Medinaceli L, Freed W J, Wyatt R J. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks.  Exp Neurol. 1982;  77 634-643
• 31 Bain J R, Mackinnon S E, Hunter D A. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat.  Plast Reconstr Surg. 1989;  83 129-138
• 32 Hare G M, Evans P J, Mackinnon S E et al.. Walking track analysis: utilization of individual footprint parameters.  Ann Plast Surg. 1993;  30 147-153
• 33 Reynolds J L, Urbanchek M S, Asato H, Kuzon Jr W M. Deletion of individual muscles alters rat walking-track parameters.  J Reconstr Microsurg. 1996;  12 461-466
• 34 Belin B M, Ball D J, Langer J C, Bridge P M, Hagberg P K, Mackinnon S E. The effect of age on peripheral motor nerve function after crush injury in the rat.  J Trauma. 1996;  40 775-777
• 35 Terzis J K, Smith K J. Repair of severed peripheral nerves: comparison of the “de Medinaceli” and standard microsuture methods.  Exp Neurol. 1987;  96 672-680
• 36 Dellon E S, Dellon A L. Functional assessment of neurologic impairment: track analysis in diabetic and compression neuropathies.  Plast Reconstr Surg. 1991;  88 686-694
• 37 Hare G M, Evans P J, Mackinnon S E et al.. Walking track analysis: a long-term assessment of peripheral nerve recovery.  Plast Reconstr Surg. 1992;  89 251-258
• 38 Kobayashi J, Mackinnon S E, Watanabe O et al.. The effect of duration of muscle denervation on functional recovery in the rat model.  Muscle Nerve. 1997;  20 858-866
• 39 McCallister W V, Tang P, Smith J, Trumble T E. Axonal regeneration stimulated by the combination of nerve growth factor and ciliary neurotrophic factor in an end-to-side model.  J Hand Surg. 2001;  26A 478-488
• 40 Terris D J, Cheng E T, Utley D S, Tarn D M, Ho P R, Verity A N. Functional recovery following nerve injury and repair by silicon tubulization: comparison of laminin-fibronectin, dialyzed plasma, collagen gel, and phosphate buffered solution.  Auris Nasus Larynx. 1999;  26 117-122
• 41 Yan J G, Matloub H S, Sanger J R, Zhang L L, Riley D A, Jaradeh S S. A modified end-to-side method for peripheral nerve repair: large epineurial window helicoid technique versus small epineurial window standard end-to-side technique.  J Hand Surg. 2002;  27A 484-492
• 42 Malushte T S, Kerns J M, Huang C C, Shott S, Safanda J, Gonzalez M. Assessment of recovery following a novel partial nerve lesion in a rat model.  Muscle Nerve. 2004;  30 609-617
• 43 Zimmermann M. Pathobiology of neuropathic pain.  Eur J Pharmacol. 2001;  429 23-37
• 44 Lindenlaub T, Sommer C. Partial sciatic nerve transection as a model of neuropathic pain: a qualitative and quantitative neuropathological study.  Pain. 2000;  89 97-106
• 45 Seltzer Z, Dubner R, Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury.  Pain. 1990;  43 205-218
• 46 Rothwell N J, Hopkins S J. Cytokines and the nervous system II. Actions and mechanisms of action.  Trends Neurosci. 1995;  18 130-136
• 47 Kato S IC. Axonal sprouting at the node of Ranvier of the peripheral nerve disconnected with the cell body.  Restor Neurol Neurosci. 1994;  6 181-187
• 48 Scherman P, Lundborg G, Kanje M, Dahlin L B. Neural regeneration along longitudinal polyglactin sutures across short and extended defects in the rat sciatic nerve.  J Neurosurg. 2001;  95 316-323
• 49 Vrbova G, Gordon R, Jones R. Re-innervation of the Muscle by its Motor Nerve. Nerve-Muscle Interaction London; Chapman and Hall 1978: 105-118
• 50 Barini O. End-to-side neurorrhaphy with and without perineurium.  Sao Paulo Med J / Rev Paul Med. 2002;  120 93-95
• 51 Kerns J M, Danielsen N, Holmquist B, Kanje M, Lundborg G. The influence of predegeneration on regeneration through peripheral nerve grafts in the rat.  Exp Neurol. 1993;  122 28-36
• 52 Caplan J, Tiangco D A, Terzis J K. Effects of IGF-II in a new end-to-side model.  J Reconstr Microsurg. 1999;  15 351-358
• 53 Bervar M. Video analysis of standing-an alternative footprint analysis to assess functional loss following injury to the rat sciatic nerve.  J Neurosci Methods. 2000;  102 109-116
• 54 Varejao A S, Cabrita A M, Patricio J A et al.. Functional assessment of peripheral nerve recovery in the rat: gait kinematics.  Microsurgery. 2001;  21 383-388
• 55 Varejao A S, Meek M F, Ferreira A J, Patricio J A, Cabrita A M. Functional evaluation of peripheral nerve regeneration in the rat: walking track analysis.  J Neurosci Methods. 2001;  108 1-9
• 56 Shen N, Zhu J. Application of sciatic functional index in nerve functional assessment.  Microsurgery. 1995;  16 552-555
• 57 de Medinaceli L. Interpreting nerve morphometry data after experimental traumatic lesions.  J Neurosci Methods. 1995;  58 29-37
• 58 Buehler M J, Seaber A V, Urbaniak J R. The relationship of functional return to varying methods of nerve repair.  J Reconstr Microsurg. 1990;  6 61-69
• 59 Dellon A L, Mackinnon S E. Selection of the appropriate parameter to measure neural regeneration.  Ann Plast Surg. 1989;  23 197-202
• 60 Munro C A, Szalai J P, Mackinnon S E, Midha R. Lack of association between outcome measures of nerve regeneration.  Muscle Nerve. 1998;  21 1095-1097
• 61 Kanaya F, Firrell J C, Breidenbach W C. Sciatic function index, nerve conduction tests, muscle contraction, and axon morphometry as indicators of regeneration.  Plast Reconstr Surg. 1996;  98 1264-1271
• 62 Kerns J M, Daugherty S R, Gramm J A, Oldershaw J B. Which measures best evaluate nerve regeneration and motor recovery following treatment with DC electric fields?. Presented at the 16th Annual Meeting, BEMS Copenhagen, Denmark; June 12-17, 1994
• 63 Kerns J M, Sladek E H, Malushte T S et al.. End-to-side nerve grafting of the tibial nerve to bridge a neuroma-in-continuity.  Microsurgery. 2005;  25 155-164