Fixed-diameter polyethylene cuffs applied to the rat sciatic nerve induce a painful neuropathy: Ultrastructural morphometric analysis of axonal alterations

Pain

Volumn 64, Issue 1, 1996, Pages 37-57

  Mosconi, Tony ^a,b   Kruger, Lawrence ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Allodynia; Axonal degeneration; Electron microscopy; Hyperalgesia; Sensory neuropathy

Indexed keywords

POLYETHYLENE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; MALE; NERVE DEGENERATION; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; ULTRASTRUCTURE;

EID: 0030032724     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/0304-3959(95)00077-1     Document Type: Article

References (77)

1. Albers, K., Wright, D.E. and Davis, B.M., Overexpression of nerve growth factor in epidermis of transgenic mice causes skin hyperinnervation and hypertrophy of trigeminal ganglion, Soc. Neurosci. Abst., 18 (1992) 1288.
2. Asbury, A.K. and Fields, H.L., Pain due to peripheral nerve damage: an hypothesis, Neurology, 34 (1984) 1587-1590.
3. Attal N., Jazat, F., Kayser, V. and Guilbaud, G., Further evidence for 'pain-related' behaviours in a model of unilateral peripheral mononeuropathy, Pain, 41 (1990a) 235-251.
4. Attal, N., Neil, A., Chen, L. and Guilbaud, G., Effects of adrenergic depletion with guanethidine before and after the induction of a peripheral neuropathy on subsequent mechanical-, heat-, and cold sensitivities in rats, Pain, Suppl. 5 (1990b) 5464.
5. Balercia, G., Mosconi, T., Anderson, D. and Kruger, L., The response of perineurial epithelium to application of fixed diameter sleeves inducing a painful neuropathy in rats. ENA Abstr., (1993) 151.
6. Basbaum, A.I., Gautron, M., Jazat, F., Mayes, M., and Guilbaud, G., The spectrum of fiber loss in a model of neuropathic pain in the rat: an electron microscopic study, Pain, 47 (1991) 359-367.
7. Benarroch, E.E., Zollman, P.J., Schmelzer, J.D., Nelson, D.K. and Low, P.A., Guanethidine sympathectomy increases substance P concentration in the superior sympathetic ganglion in adult rats, Brain Res., 584 (1992) 305-308.
8. Bennett, G.J., The role of the sympathetic nervous system in painful peripheral neuropathy, Pain, 45 (1991) 221-223.
9. Bennett, G.J. and Xie, Y.-K., A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man, Pain, 33 (1988) 87-107.
10. Bove, G.M. and Light, A.R., Paraspinal nociceptive primary afferents, Soc. Neurosci. Abstr., 18 (1992) 384.
11. Britland, S.T., Young, R.J., Sharma, A.K. and Clarke, B.F., Association of painful and painless diabetic polyneuropathy with different patterns of nerve fiber degeneration and regeneration, Diabetes, 39 (1990) 898-908.
12. Britland, S.T., Young, R.J., Sharma, A.K. and Clarke, B.F., Acute and remitting painful diabetic polyneuropathy: a comparison of peripheral nerve fibre pathology, Pain, 48 (1992) 361-370.
13. Burgess, P.R. and Perl, E.R., Cutaneous mechanoreceptors and nociceptors. In: A. Iggo (Ed.), Handbook of Sensory Physiology. Vol. II, Somatosensory System, Springer, New York, 1973, pp. 29-78.
14. Carlton, S.M., Dougherty, P.M., Pover, C.M. and Coggeshall, R.E., Neuroma formation and numbers of axons in a rat model of experimental peripheral neuropathy, Neurosci. Lett., 131 (1991) 88-92.
15. Chaudry, V., Glass, J.D. and Griffin, J.W., Wallerian degeneration in peripheral nerve disease. In: Neurologic Clinics, Peripheral Neuropathy: New Concepts and Treatments, W.B. Saunders, Philadelphia, PA, Vol. 10, 1992, pp. 613-627.
16. Chung, J.M., Leem, J.W. and Kim, S.H., Somatic afferent fibers which continuously discharge after being isolated from their receptors, Brain Res., 599 (1992) 29-33.
17. Chung, K., Kim, H.J., Na, H.S., Park, M.J. and Chung, J.M., Abnormalities of sympathetic innervation in the area of an injured peripheral nerve in a rat model of neuropathic pain, Neurosci. Lett., 162 (1993) 85-88.
18. Coderre, T.J. and Melzack, R., Cutaneous hyperalgesia: contributions of the peripheral and central nervous systems to the increase in pain sensitivity after injury, Brain Res., 404 (1987) 95-106.
19. Coggeshall, R.E., Dougherty, P.M., Pover, C.M. and Carlton, S.M., Is large myelinated fiber loss associated with hyperalgesia in a model of experimental peripheral neuropathy in the rat?, Pain, 52 (1993) 233-242.
20. Devor, M., Nerve pathophysiology and mechanisms of pain in causalgia, J. Autonom. Nerv. Syst., 7 (1983) 371-384.
21. Diamond, J., Foerster, A., Holmes, M. and Coughlin, M., Sensory nerves in adult rats regenerate and restore function to the skin independently of endogenous NGF, J. Neurosci., 12 (1992a) 1467-1476.
22. Diamond, J., Holmes, M. and Coughlin, M., Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat, J. Neurosci., 12 (1992b) 1454-1466.
23. Dyck, P.J., Lambert, E.H., and O'Brien, P.C., Pain in peripheral neuropathy related to rate and kind of fiber degeneration, Neurology, 26 (1976) 466-471.
24. Dyck, P.J., Thomas, P.K., Lambert, E.H. and Bunge, R. (Eds.), Peripheral Neuropathy, Vol. 1, W.B. Saunders, Philadelphia, PA, 1984, 1165 pp.
25. Dyck, P.J., Lais, A.C., Giannini, C. and Engelstad, J.K., Structural alterations of nerve during cuff compression, Proc. Natl. Acad. Sci. USA, 87 (1990) 9828-9832.
26. Fried, K., Govrin-Lippmann, R. and Devor, M., Close apposition among neighbouring axonal endings in a neuroma, J. Neurocytol., 22 (1993) 663-681.
27. Garrison, C.J., Dougherty, P.M. and Carlton, S.M., Quantitative analysis of substance P and calcitonin gene-related peptide immunohistochemical staining in the dorsal horn of neuropathic MK-80 1-treated rats, Brain Res., 607 (1991) 205-214.
28. Gautron, M., Jazat, F., Ratinahirana, H., Hauw, J.J. and Guilbaud, G., Alterations in myelinated fibers in the sciatic nerve of rats after constriction: possible relationships between the presence of abnormal small myelinated fibres and pain behaviour, Neurosci. Lett., 111 (1990) 28-33.
29. Guilbaud, G., Gautron, M., Jazat, F., Ratinahirana, H., Hassig, R., and Hauw, J.J., Time course of degeneration and regeneration of myelinated nerve fibres following chronic loose ligatures of the rat sciatic nerve: can nerve lesions be linked to the abnormal pain-related behaviours?, Pain, 53 (1993) 147-158.
30. Gunderson, R.W., Sensory neurite growth and guidance by substrate absorbed NGF, J. Neurosci. Res., 13 (1985) 199-212.
31. Gunderson, R.W. and Barrett, J.N., Characterization of the turning response of dorsal root neurites toward nerve growth factor, J. Cell Biol., 87 (1980) 546-554.
32. Heumann, R., Kosching, S., Bandtlow, C. and Thoenen, H., Changes in nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection, J. Cell Biol., 104 (1987a) 1623-1631.
33. Heumann, R., Lindholm, D., Bandtlow, C., Meyer, M., Radeke, M.J., Misko, T.P., Shooter, E. and Thoenen, H., Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages, Proc. Natl. Acad. Sci. USA, 84 (1987b) 8735-8739.
34. Hromoda, J., On the nerve supply of the connective tissue of some peripheral nervous system components, Acta. Anat., 55 (1963) 343-351.
35. Jenq, C.-B. and Coggeshall, R.E., Long-term patterns of axon regeneration in the sciatic nerve and its tributaries, Brain Res., 345 (1985) 34-44.
36. Kajander, K.C. and Bennett, G.J., Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in Aβ and Aδ primary afferent neurons, J. Neurophysiol., 68 (1992) 734-744.
37. Kajander, K.C., Wakisaka, S. and Bennett, G.J., Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat, Neurosci. Lett., 138 (1992) 225-228.
38. Kim, S.H. and Chung, J.M., An experimental model for peripheral mononeuropathy produced by segmental spinal nerve ligation in the rat, Pain, 50 (1992) 355-362.
39. Laird, J.M.A. and Bennett, G.J., Dorsal root potentials and afferent input to the spinal cord in rats with an experimental peripheral neuropathy, Brain Res., 584 (1992) 181-190.
40. Laird, J.M.A. and Bennett, G.J., An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy, J. Neurophysiol., 69 (1993) 2072-2085.
41. Lewin, G.R. and Mendell, L.M., Nerve growth factor and nociception, TINS, 16 (1993) 353-359.
42. Lewin, G.R., Ritter, A.M. and Mendell, L.M., Nerve growth factor-induced hyperalgesia in neonatal and adult rat, J. Neurosci., 13 (1993) 2136-2148.
43. Llewelyn, J.G., Gilbey, S.G., Thomas, P.K., King, R.H., Muddle, J.R. and Watkins, P.J., Sural nerve morphometry in diabetic autonomic and painful sensory neuropathy. A clinicopathological study, Brain, 114 (1991) 867-892.
44. Mao, J., Price, D.D., Mayer, D.J., Lu, J. and Hayes, R.L., Intrathecal MK-801 and local nerve anesthesia synergistically reduce nociceptive behaviors in rats with experimental peripheral neuropathy, Brain Res., 576 (1992) 254-262.
45. Maves, T.J., Pechman, P.S., Gebhart, G.F. and Meller, S.T., Mechanisms of neuropathic pain following chromic gut ligation of the sciatic nerve in the rat, Soc. Neurosci. Abstr., 18 (1992) 285.
46. Maves, T.J., Pechman, P.S., Gebhart, G.F. and Meller, S.T., Possible chemical contribution from chromic gut sutures produces disorders of pain sensation like those seen in man, Pain, 54 (1993a) 57-69.
47. Maves, T.J., Pechman, P.S., Gebhart, G.F., and Meller, S.T., Continuous infusion of acidified saline around the rat sciatic nerve produces a reversible thermal hyperalgesia, IASP 7th World Congress Abstr., 1993b, p. 31.
48. Mazurek, N., Weskamp, G., Erne, P. and Otten, U., Nerve growth factor induces mast cell degranulation without changing intracellular calcium levels, FEBS Lett., 198 (1986) 315-320.
49. Mearow, K.M., Kril, Y. and Diamond, J., Increased NGF mRNA expression in denervated rat skin, NeuroReport, 4 (1993) 351-354.
50. Meller, S.T., Gebhart, G.F. and Maves, T.J., Neonatal capsaicin treatment prevents the development of the thermal hyperalgesia produced in a model of neuropathic pain in the rat, Pain, 51 (1992) 317-321.
51. Mosconi, T. and Kruger, L., Electron microscopic analysis of axon fiber spectrum following neuropathy induced by fixed-diameter nerve constriction, Soc. Neurosci. Abstr., 18 (1992) 289.
52. Mosconi, T., Lue, P., McNally, E., Anderson, D., McDonald, J. and Kruger, L., Immunohistochemical and electron microscopic studies of cuff-induced painful mononeuropathy, Soc. Neurosci. Abst., 20 (1994) 151.
53. Munger, B.L., Bennett, G.J. and Kajander, K.C., An experimental painful peripheral neuropathy due to nerve constriction. I. Axonal pathology in the sciatic nerve, Exp. Neurol., 118 (1992) 204-214.
54. Myers, R.R., Rydevik, B.L., Heckman, H.M. and Powell, H.C., Proximodistal gradient in endoneurial fluid pressure, Exp. Neurol., 102 (1988) 368-370.
55. Myers, R.R., Yamamoto, T., Yaksh, T.L. and Powell, H.C., The role of focal nerve ischemia and Wallerian degeneration in peripheral nerve injury producing hyperesthesia, Anesthesiology, 78 (1993) 306-316.
56. Neil, A., Attal, N. and Guilbaud, G., Effects of guanethidine on sensitization to natural stimuli and self-mutilating behaviour in rats with a peripheral neuropathy, Brain Res., 565 (1991) 237-246.
57. Nuytten, D., Kupers, R., Lammens, M., Dom, R., van Hees, J. and Gybels, J., Further evidence for myelinated as well as unmyelinated fibre damage in a rat model of neuropathic pain, Exp. Brain Res., 91 (1992) 73-78.
58. Perrot, S., Attal, N., Ardid, D. and Guilbaud, G., Are mechanical and cold allodynia in mononeuropathic and arthritic rats relieved by systemic treatment with calcitonin or guanethidine?, Pain, 51 (1993) 41-47.
59. Powell, H.C., Myers, R.R., Costello, M.L. and Lampert, P.W., Endoneurial fluid pressure in Wallerian degeneration, Ann. Neurol., 5 (1979) 550-557.
60. Pryor, J.C., Horigome, K. and Johnson, E.M. Jr., Mast cells express TRK but not low affinity nerve growth factor receptor, Soc. Neurosci. Abst., 18 (1992) 952.
61. Raivich, G., Hellweg, R. and Kreutzberg, G.W., NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury and during regeneration, Neuron, 7 (1991) 151-164.
62. Ro, L.-S. and Jacobs, J.M., The role of the saphenous nerve in experimental sciatic nerve mononeuropathy produced by loose ligatures: a behavioural study, Pain, 52 (1993) 359-369.
63. Robbins, S.L., Pathologic basis of disease, W.B. Saunders, Philadelphia, PA, 1974, 1143 pp.
64. Sato, J. And Perl, E.R., Adrenergic excitation of cutaneous pain receptors induced by peripheral nerve injury, Science, 251 (1991) 1608-1610.
65. Seltzer, Z., Dubner, R. and Shir, Y., A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury, Pain, 43 (1990) 205-218.
66. Shir, Y. and Seltzer, Z., A-fibers mediate mechanical hyperesthesia and allodynia and C-fibers mediate thermal hyperalgesia in a new model of causalgiaform pain disorders in rats, Neurosci. Lett., 115 (1990) 62-67.
67. Silverman, J.D. and Kruger, L., An interpretation of dental innervation based upon the pattern of calcitonin gene-related peptide (CGRP)-immunoreactive thin sensory axons, Somatosens. Res., 5 (1987) 157-175.
68. Somer, C. and Myers, R.R., Pathology of experimental constriction neuropathy: comparison of histopathology and hyperalgesia in different rodent models, IASP 7th World Congress Abst., 1993, p. 30.
69. Stewart, J.D. and Aguayo, A.J., Compression and entrapment neuropathies. In: P.J. Dyck, E.H. Lambert, and R. Bunge (Eds.), Peripheral Neuropathy, W.B. Saunders, Company,Philadelphia, PA, 1984, pp. 1435-1457.
70. Swett, J.E., Wikholm, R.P., Blanks, R.H.I., Swett, A.L. and Conley, L.C., Motoneurons of the rat sciatic nerve, Exp. Neurol., 93 (1986) 227-252.
71. Tanck, E.N., Kroin, J.S., McCarthy, R.J., Penn, R.D. and Ivankovich, A.D., Effects of age and size on development of allodynia in a chronic pain model produced by sciatic nerve ligation in rats, Pain, 51 (1992) 313-316.
72. Taniuchi, M., Clark, H.B., and Johnson, E.M. Jr., Induction of nerve growth factor receptor in Schwann cells after axotomy, Proc. Nat. Acad. Sci. USA, 83 (1986) 4094-4098.
73. Taniuchi, M., Clark, H.B., Schweitzer, J.B. and Johnson, E.M., Jr., Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural localization, suppression by axonal contact, and binding properties, J. Neurosci., 8 (1988) 664-681.
74. Treede, R.-D. and Cole, J.D., Dissociated secondary hyperalgesia in a subject with large-fibre sensory neuropathy, Pain, 53 (1993) 169-174.
75. Urschel, B.A. and Hulsebosch, C.E., Schwann cell-neuronal interactions in rat involve nerve growth factor, J. Comp. Neurol., 296 (1990) 114-122.
76. Weisl, H. and Osborne, G.V., The pathological changes in rats' nerves subject to moderate compression, J. Bone Joint Surg., 46 (1964) 297-306.
77. Zochodne, D.W., Epineurial peptides: a role in neuropathic pain?, Can. J. Neurol. Sci., 20 (1993) 69-72.