Methods for the experimental functional assessment of rat sciatic nerve regeneration

Neurological Research

Volumn 26, Issue 2, 2004, Pages 186-194

  Varejão, Artur S P ^a,c   Melo Pinto, Pedro ^a   Meek, Marcel F ^b   Filipe, Vitor M ^a   Bulas Cruz, José ^a  

^a UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

Computer gait analysis; Functional recovery; Rat; Sciatic nerve

Indexed keywords

ANIMAL MODEL; FUNCTIONAL ASSESSMENT; GAIT; GASTROCNEMIUS MUSCLE; KINEMATICS; MUSCLE MASS; NERVE REGENERATION; NONHUMAN; RAT; REVIEW; SCIATIC NERVE; SOLEUS MUSCLE; WALKING;

ANIMALS; BIOMECHANICS; NERVE REGENERATION; RATS; RECOVERY OF FUNCTION; RESEARCH DESIGN; SCIATIC NERVE; WALKING;

EID: 1842607174     PISSN: 01616412     EISSN: None     Source Type: Journal    
DOI: 10.1179/016164104225013833     Document Type: Review

References (116)

1. de Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 1982; 77: 634-643
2. Dellon AL, Mackinnon SE. Selection of the appropriate parameter to measure neural regeneration. Ann Plast Surg 1989; 23: 197-202
3. Shen N, Zhu J. Application of sciatic functional index in nerve functional assessment. Microsurgery 1995; 16: 552-555
4. Di Cataldo A, La Greca G, Rodolico M, Candiano C, Li Destri G, Puleo S. Experimental models in microsurgery. Microsurgery 1998; 18: 454-459
5. Bertelli JA, Mira JC. The grasping test: a simple behavioral method for objective quantitative assessment of peripheral nerve regeneration in the rat. J Neurosci Meth 1995; 58: 151-155
6. Bontioti EN, Kanje M, Dahlin LB. Regeneration and functional recovery in the upper extremity of rats after various types of nerve injuries. J Periph Nerv Syst 2003; 8: 159-168
7. Papalia I, Tos P, d'Alcontres FS, Battiston B, Geuna S. On the use of the grasping test in the rat median nerve model: a re-appraisal of its efficacy for quantitative assessment of motor function recovery. J Neurosci Meth 2003; 127: 43-47
8. Aldskogius H, Thomander L. Selective reinnervation of somatotopically appropriate muscles after facial nerve transection and regeneration in the neonatal rat. Brain Res 1986; 375: 126-134
9. Jergovic D, Stal P, Lidman D, Lindvall B, Hildbrand C. Changes in a rat facial muscle after facial nerve injury and repair. Muscle Nerve 2001; 24: 1202-1212
10. Back SK, Sung B, Hong SK, Na HS. A mouse model for peripheral neuropathy produced by a partial injury of the nerve supplying the tail. Neurosci Lett 2002; 322: 153-156
11. Lee WP, Constantinescu MA, Butler PE. Effect of early mobilization on healing of nerve repair: histologic observations in a canine model. Plast Reconstr Surg 1999; 104: 1718-1725
12. Matsumoto K, Ohnishi K, Kiyotani T, Sekine T, Ueda H, Nakamura T, Endo K, Shimizu Y. Peripheral nerve regeneration across an 80-mm gap bridged by polyglycolic acid (PGA)-collagen tube filled with laminin-coated collagen fibers: a histological and electrophysiological evaluation of regenerated nerves. Brain Res 2000; 868: 315-328
13. Suzuki Y, Tanihara M, Ohnishi K, Suzuki K, Endo K, Nishimura Y. Cat peripheral nerve regeneration across 50 mm gap repaired with a novel nerve guide composed of freeze-dried alginate gel. Neurosci Lett 1999; 259: 75-78
14. Heijke GCM, Klopper PJ, Van Doorn IBM, Baljet B. Processed porcine collagen tubulization versus conventional suturing in peripheral nerve reconstruction: an experimental study in rabbits. Microsurgery 2001; 21: 84-95
15. Sarikcioglu L, Oguz N. Exercise training and axonal regeneration after sciatic nerve injury. Int J Neurosci 2001; 109: 173-177
16. Lawson GM, Glasby MA. Peripheral nerve reconstruction using freeze-thawed muscle grafts: a comparison with group fascicular nerve grafts in a large animal model. J Roy Coll Surg Edin 1998; 43: 295-302
17. Glasby MA, Gilmour JA, Gschmeissner SE, Hems TEJ, Myles LM. The repair of large peripheral nerves using skeletal muscle autografts: a comparison with cable grafts in the sheep femoral nerve. Br J Plast Surg 1990; 43: 169-178
18. Mackinnon SE, Dellon AL. A study of nerve regeneration across synthetic (maxon) and biologic (collagen) nerve conduits for nerve gaps up to 5cm in the primate. J Reconstr Surg 1990; 6: 117-121
19. Archibald SJ, Shefner J, Krarup C, Madinson RD. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. J Neurosci 1995; 15: 4109-4123
20. Munro CA, Szalai JP, Mackinnon SE, Midha R. Lack of association between outcome measures of nerve regeneration. Muscle Nerve 1998; 21: 1095-1097
21. Wong BJ, Mattox DE. Experimental nerve regeneration. A review. Otolaryngol Clin North Am 1991; 24: 739-752
22. Kanaya F, Firrell JC, Breidenbach WC. Sciatic function index, nerve conduction tests, muscle contraction, and axon morphometry as indicators of regeneration. Plast Reconstr Surg 1996; 98: 1264-1271
23. Mackinnon SE. Sciatic function index, nerve conduction tests, muscle contraction, and axon morphometry as indicators of regeneration-Discussion. Plast Reconstr Surg 1996; 98: 1272-1274
24. Hadlock T, Koka R, Vacanti J, Cheney M. A comparison of assessments of functional recovery in the rat. J Periph Nerv Syst 1999; 4: 258-264
25. Carlton JM, Goldberg NH. Quantitating integrated muscle function following reinnervation. Surg Forum 1986; 37: 611-612
26. Bain JR, Mackinnon SE, Hunter DA. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 1989; 83: 129-136
27. Babovic S, Ress AM, Dellon AL, Angel MF, Im MJ, Manson PN. Nerve regeneration in diabetic rats. Microsurgery 1998; 18: 9-11
28. Castañeda F, Kinne RKH. Omental graft improves functional recovery of transected peripheral nerve. Muscle Nerve 2002; 26: 527-532
29. Cudlip SA, Howe FA, Griffiths JR, Bell BA. Magnetic resonance neurography of peripheral nerve following experimental crush injury, and correlation with functional deficit. J Neurosurg 2002; 96: 755-759
30. Islamov RR, Hendricks WA, Jones RJ, Lyall GL, Spanier NS, Murashov AK. 17β-Estradiol stimulates regeneration of sciatic nerve in female mice. Brain Res 2002; 943: 283-286
31. Ayhan S, Markal N, Siemionow K, Araneo B, Siemionow M. Effect of subepineurial dehydroepiandrosterone treatment or healing of transected nerves repaired with epineurial slee technique. Microsurgery 2003; 23: 49-55
32. Brown CJ, Mackinnon SE, Evans PJ, Bain JR, Makino AP, Hunter DA, Hare GMT. Self-evaluation of walking-track measurement using a sciatic function index. Microsurgery 1989; 10: 226-235
33. Strasberg SR, Watanabe O, Mackinnon SE, Tarasidis G, Hertl MC, Wells MR. Wire mesh as a post-operative physiotherapy assistive device following peripheral nerve graft repair in the rat. J Periph Nerv Syst 1996; 1: 73-76
34. Kobayashi J, Mackinnon SE, Watanabe O, Ball DJ, Gu XM, Hunter DA, Kuzon WM Jr. The effect of duration of muscle denervation on functional recovery in the rat model. Muscle Nerve 1997; 20: 858-866
35. Meek MF, Den Dunnen WFA, Schakenraad JM, Robinson PH. 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. Microsurgery 1999; 19: 247-253
36. Meek MF, den Dunnen WF, Bartels HL, Pennings AJ, Robinson PH, Schakenraad JM. Peripheral nerve regeneration and functional nerve recovery after reconstruction with a thin-walled biodegradable poly(DL-lactide-ε -caprolactone) nerve guide. Cells Mater 1997; 7: 53-62
37. Lowdon IMR, Seaber AV, Urbaniak JR. An improved method of recording rat tracks for measurement of the sciatic functional index of de Medinaceli. J Neurosci Meth 1988; 24: 279-281
38. Zellem RT, Miller DW, Kenning JA, Hoening EM, Buchheit WA. Experimental peripheral nerve repair: environmental control directed at the cellular level. Microsurgery 1989; 10: 290-301
39. van Meeteren NLU, Brakkee JH, Hamers FPT, Helders PJM, Gispen WH. Exercise training improves functional recovery and motor nerve concuction velocity after sciatic nerve crush lesion in the rat. Arch Phys Med Rehabil 1997; 78: 70-77
40. Dijkstra JR, Meek MF, Robinson PH, Gramsbergen A. Methods to evaluate functional nerve recovery in adult rats: walking track analysis, video analysis and the withdrawal reflex. J Neurosci Meth 2000; 96: 89-96
41. Kanaya F, Firrell J, Tsai T-M, Breidenbach WC. Functional results of vascularized versus nonvascularized nerve grafting. Plast Reconstr Surg 1992; 89: 924-930
42. Terris DJ, Cheng ET, Utley DS, Tarn DM, Ho PR, Verity NA. Functional recovery following nerve injury and repair by silicon tubulization: comparison of laminin-fibronectin, dialyzed plasma, collagen gel, and a phosphate buffered solution. Auris Nasus Larynx 1999; 26: 117-122
43. Reynolds JL, Urbanchek MS, Asato H, Kuzon WM Jr. Deletion of individual muscles alters rat walking-track parameters. J Reconstr Microsurg 1996; 12: 461-466
44. Valero-Cabré A, Navarro X. H reflex restitution and facilitation after different types of peripheral nerve injury and repair. Brain Res 2001; 919: 302-312
45. Inserra MM, Bloch DA, Terris DJ. Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery 1998; 18: 119-124
46. Hare GMT, Evans PJ, Mackinnon SE, Best TJ, Bain JR, Szalai JP, Hunter DA. Walking track analysis: A long-term assessment of peripheral nerve recovery. Plast Reconstr Surg 1992; 89: 251-258
47. Maeda T, Mackinnon SE, Best TJ, Evans PJ, Hunter DA, Rajiv Midha RT. Regeneration across "stepping-stone" nerve grafts. Brain Res 1993; 618: 196-202
48. de Medinaceli L, DeRenzo E, Wyatt RJ. Rat sciatic functional index data management system with digitized input. Comput Biomed Res 1984; 17: 185-192
49. Dellon ES, Dellon AL. Functional assessment of neurological impairment: track analysis in diabetic and compression neuropathies. Plast Reconstr Surg 1991; 88: 686-694
50. Oliveira EF, Mazzer N, Barbieri CH, Selli M. Correlation between functional index and morphometry to evaluate recovery of the rat sciatic nerve following crush injury: experimental study. J Reconstr Microsurg 2001; 17: 69-75
51. Terzis JK, Smith KJ. Repaired of severed peripheral nerves: comparison of the "de Medinaceli" and standard microsuture methods. Exp Neurol 1987; 96: 672-680
52. Hirasé Y, Kojima T, Uchida M, Takeishi M. Cryopreserved allogeneic vessel and nerve grafts: hind-limb replantation model in the rat. J Reconstr Microsurg 1992; 8: 437-443
53. Pu LL, Syed SA, Reid M, Patwa H, Goldstein JM, Forman DL, Thomson JG. Effects of nerve growth factor on nerve regeneration through a vein graft across a gap. Plast Reconstr Surg 1999; 104: 1379-1385
54. Hoogeveen JF, Troost D, Wondergem J, van der Kracht AHW, Haveman J. Hyperthermic injury versus crush injury in the rat sciatic nerve: a comparative functional, histopathological and morphometric study. J Neurol Sci 1992; 108: 55-64
55. Menovsky T, Beek JF. Laser, fibrin glue, or suture repair of peripheral nerves: a comparative functional, histological, and morphometric study in the rat sciatic nerve. J Neurosurg 2001; 95: 694-699
56. Shenaq JM, Shenaq SM, Spira M. Reliability of sciatic function index in assessing nerve regeneration across a 1 cm gap. Microsurgery 1989; 10: 214-219
57. Weber RA, Warner MR, Verheyden CN, Proctor WH. Functional evaluation of gaps vs. abutment repair of peripheral nerves in the rat. J Reconstr Microsurg 1996; 12: 159-163
58. Chamberlain LJ, Yannas IV, Hsu H-P, Strichartz GR, Spector M. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a Collagen-GAG matrix in a ten-milimeter gap. J Neurosci Res 2000; 60: 666-677
59. Varejão ASP, Cabrita AM, Geuna S, Patricio JA, Azevedo HR, Ferreira AJ, Meek MF. Functional assessment of sciatic nerve recovery: biodegradable poly (DLLA-ε-CL) nerve guide filled with fresh skeletal muscle. Microsurgery 2003; 23: 346-353
60. Kauppila T. Correlation between autotomy-behavior and current theories of neuropathic pain. Neurosci Biobehav Rev 1998; 23: 111-129.
61. Den Dunnen WFA, Meek MF. Sensory nerve function and auto-mutilation after reconstruction of various gap lengths with nerve guides and autologous nerve grafts. Biomaterials 2001; 22: 1171-1176
62. Sporel-Ozakat RE, Edwards PM, Hepgul KT, Savas A, Gispen WH. A simple method for reducing autotomy in rats after peripheral nerve lesions. J Neurosci Meth 1991; 36: 263-265
63. Navarro X, Butí M, Verdú E. Autotomy prevention by amitriptyline after peripheral nerve section in different strains of mice. Rest Neurol Neurosci 1994; 6: 151-157
64. Carr MM, Best TJ, Mackinnon SE, Evans PJ. Strain differences in autotomy in rats undergoing sciatic nerve transection or repair. Ann Plast Surg 1992; 28: 538-544
65. Valero-Cabré A, Navarro X. Functional impact of axonal misdirection after peripheral nerve injuries followed by graft or tube repair. J Neurotrauma 2002; 19: 1475-1485
66. Gramsbergen A, IJkema-Paassen J, Meek MF. Sciatic nerve transection in the adult rat: abnormal EMG patterns during locomotion by aberrant innervation of hindleg muscles. Exp Neurol 2000; 161: 183-193
67. IJkema-Paassen J, Meek MF, Gramsbergen A. Muscle differentiation after sciatic nerve transection and reinnervation in adult rats. Ann Anat 2001; 183: 369-377
68. IJkema-Paassen J, Meek MF, Gramsbergen A. Reinnervation of muscles after transection of the sciatic nerve in adult rats. Muscle Nerve 2002; 25: 891-897
69. Thalhammer JG, Vladimirova M, Bershadsky B, Strichartz GR. Neurologic evaluation of the rat during sciatic nerve block with lidocaine. Anesthesiology 1995; 82: 1013-1025
70. Koka R, Hadlock T. Quantification of functional recovery following rat sciatic nerve transection. Exp Neurol 2001; 168: 192-195
71. Howard CS, Blakeney DC, Medige J, Moy OJ, Peimer CA. Functional assessment in the rat by ground reaction forces. J Biomechanics 2000; 33: 751-757
72. Muir GD, Webb AA. Mini-review: assessment of behavioural recovery following spinal cord injury in rats. Eur J Neurosci 2000; 12: 3079-3086
73. Clarke KA, Smart L, Still J. Ground reaction force and spatiotemporal measurements of the gait of the mouse. Behav Res Methods Instrum Comput 2001; 33: 422-426
74. Schmalbruch H. Fiber composition of the rat sciatic nerve. Anat Rec 1986; 215: 71-81
75. Millan MJ. The induction of pain: an integrative review. Prog Neurobiol 1999; 57: 1-164
76. Craig AD, Andrew D. Responses of spinothalamic lamina I neurons to repeated brief contact heat stimulation in the cat. J Neurophysiol 2002; 87: 1902-1914
77. Tracey DJ. Ascending and descending pathways in the spinal cord. In: Paxinos G, ed. The rat nervous system, San Diego: Academic Press, 1995: pp. 67-80
78. Schouenborg J, Kalliomaki J. Functional organization of the nociceptive withdrawal reflexes. I. Activation of hindlimb muscles in the rat. Exp Brain Res 1990; 83: 67-78
79. Masters DB, Berde CB, Dutta SK, Griggs CT, Hu D, Kupsky W, Langer R. Prolonged regional nerve blockade by controlled release of local anesthetic from a biodegradable polymer matrix. Anesthesiology 1993; 79: 340-346
80. Hu D, Hu R, Berde CB. Neurologic evaluation of infant and adult rats before and after sciatic nerve blockade. Anesthesiology 1997; 86: 957-965
81. De Koning P, Brakkee JH, Gispen WH. 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. J Neurol Sci 1986; 74: 237-246
82. van Meeteren NLU, Brakkee JH, Helders PJM, Gispen WH. The effect of exercise training on functional recovery after sciatic nerve crush in the rat. J Periph Nerv Syst 1998; 3: 277-282
83. Devor M, Schonfeld D, Seltzer Z, Wall PD. Two modes of cutaneous reinnervation following peripheral nerve injury. J Comp Neurol 1979; 185: 211-220
84. Navarro X, Verdú E, Butí M. Comparison of regenerative and reinnervation capabilities of different functional types of nerve fibers. Exp Neurol 1994; 129: 217-224
85. Scharpf J, Meirer R, Zielinski M, Unsal M, Ramineni P, Nair D, Siemionow M. A novel technique for peripheral nerve repair. Laryngoscope 2003; 113: 95-101
86. Lee KC, Wilder RT, Smith RL, Berde CB. Thermal hyperalgesia accelerates and MK-801 prevents the development of tachyphylaxis to rat sciatic nerve blockade. Anesthesiology 1994; 81: 1284-1293
87. Castillo J, Curley J, Hotz J, Uezono M, Tigner J, Chasin M, Wilder R, Langer R, Berde C. Glucocorticoids prolong rat sciatic nerve blockade in vivo from bupivacaine microspheres. Anesthesiology 1996; 85: 1157-1166
88. Meek MF, den Dunnen WF, IJkema-Paassen J, Schakenraad JM, Gramsbergen A, Robinson PH. Functional assessment of sciatic nerve reconstruction: biodegradable poly (DLLA-c-CL) nerve guides versus autologous nerve grafts. Microsurgery 1999; 19: 381-388
89. Kingery WS, Vallin JA. The development of chronic mechanical hyperalgesia, autotomy and collateral sprouting following sciatic nerve section in rat. Pain 1989; 38: 321-332
90. Kanje M, Lundborg G, Edström A. A new method for studies of the effects of locally applied drugs on peripheral nerve regeneration in vivo. Brain Res 1988; 439: 116-121
91. Lundborg G, Dahlin L, Dohi D, Kanje M, Terada N. A new type of "bioartificial" nerve graft for bridging extended defects in nerves. J Hand Surg; 22B: 299-303
92. Arai T, Lundborg G, Dahlin LB. Bioartificial nerve graft for bridging extended nerve defects in rat sciatic nerve based on resorbable guiding filaments. Scand J Plast Reconstr Surg Hand Surg 2000; 34: 101-108
93. Meyer RS, Abrams RA, Botte MJ, Davey JP, Bodine-Fowler SC. Functional recovery following neurorrhaphy of the rat sciatic nerve by epineurial repair compared with tubulization. J Orthop Res 1997; 15: 664-669
94. Dowsing BJ, Hayes A, Bennett TM, Morrison WA, Messina A. Effects of LIF dose and laminin plus fibronectin on axotomized sciatic nerves. Muscle Nerve 2000; 23: 1356-1364
95. Sobeski JK, Kerns JM, Safanda JF, Shott S, Gonzalez MH. Functional and structural effects of GM-1 ganglioside treatment on peripheral nerve grafting in the rat. Microsurgery 2001; 21: 108-115
96. Hou Z, Zhu J. An experimental study about the incorrect electrophysiological evaluation following peripheral nerve injury and repair. Electromyogr Clin Neurophysiol 1998; 38: 301-304
97. Evans GRD, Brandt K, Widmer MS, Lu L, Meszlenyi RK, Gupta PK, Mikos AG, Hodges J, Williams J, Gurlek A, Nabawi A, Lohman R, Patrick Jr CW. In vivo evaluation of poly (L-lactic acid) porous conduits for peripheral nerve regeneration. Biomaterials 1999; 20: 1109-1115
98. Shiraishi E, Shibata M, Takahashi HE. Rat tibial nerve regeneration after postoperative administration of cis-diaminedichloroplatinum. Plast Reconstr Surg 1998; 101: 1039-1044
99. Gage JR. The clinical use of kinetics for evaluation of pathological gait in cerebral palsy. J Bone Joint Surg 1994; 76A: 622-631
100. Varejão ASP, Cabrita AMS, Patrício JA, Bulas-Cruz J, Gabriel RC, Melo-Pinto P, Couto PA, Meek MF. Functional assessment of peripheral nerve recovery in the rat: gait kinematics. Microsurgery 2001; 21: 383-388
101. Walker JL, Resig P, Guarnieri S, Sisken BF, Evans JM. Improved footprint analysis using video recording to assess functional recovery following injury to the rat sciatic nerve. Restor Neurol Neurosci 1994; 6: 189-193
102. Westerga J, Gramsbergen A. Development of locomotion in the rat. Dev Brain Res 1990; 57: 163-174
103. Meek MF, Van Der Werff JF, Nicolai J-PA, Gramsbergen A. Biodegradable p(DLLA-ε-CL) nerve guides versus autologous nerve grafts: Electromyographic and video analysis. Muscle Nerve 2001; 24: 753-759
104. Bervar M. Video analysis of standing-an alternative footprint analysis to assess functional loss following injury to the rat sciatic nerve. J Neurosci Meth 2000; 102: 109-116
105. Bervar M. An alternative video footprint analysis to assess functional loss following injury to the rat sciatic nerve. Acta Chir Plast 2002; 44: 86-89
106. Zehr EP, Stein RB. What functions do reflexes serve during human locomotion? Prog Neurobiol 1999; 58: 185-205
107. Hamers FPT, Lankhorst AJ, Van Laar TJ, Veldhuis WB, Gispen WH. Automated quantitative gait analysis during overground locomotion in the rat: Its application to spinal cord contusion and transection injuries. J Neurotrauma 2001; 18: 187-201
108. Chambers HG, Sutherland DH. A practical guide to gait analysis. J Am Acad Orthop Surg 2002; 10: 222-231
109. Walker JL, Evans JM, Meade P, Resig P, Sisken BF. Gait-stance duration as measure of injury and recovery in the rat sciatic nerve model. J Neurosci Meth 1994; 52: 47-52
110. Santos PM, Williams SL, Thomas SS. Neuromuscular evaluation using rat gait analysis. J Neurosci Methods 1995; 61: 79-84
111. Santos PM. A functional model system of an hypoxic nerve injury and its evaluation. Laryngoscope 2000; 110: 845-853
112. Yu P, Matloub HS, Sanger JR, Narini P. Gait analysis in rats with peripheral nerve injury. Muscle Nerve 2001; 24: 231-239
113. Lin FM, Pan YC, Hom C, Sabbahi M, Shenaq S. Ankle stance angle: A functional index for the evaluation of sciatic nerve recovery after complete transection. J Reconstr Microsurg 1996; 12: 173-177
114. Varejão ASP, Cabrita AM, Meek MF, Bulas-Cruz J, Gabriel RC, Filipe VM, Melo-Pinto P, Winter DA. Motion of the foot and ankle during the stance phase in rats. Muscle Nerve 2002; 26: 630-635
115. Varejão ASP, Cabrita AM, Meek MF, Bulas-Cruz J, Filipe VM, Gabriel RC, Ferreira AJ, Geuna S, Winter DA. Ankle kinematics to evaluate functional recovery in crushed rat sciatic nerve. Muscle Nerve 2003; 27: 706-714
116. Varejão ASP, Cabrita AM, Geuna S, Melo-Pinto P, Filipe VM, Gramsbergen A, Meek MF. Toe out angle: a functional index for the evaluation of sciatic nerve recovery in the rat model. Exp Neurol 2003; 183: 695-699