Increased axonal regeneration and swellings in intraepidermal nerve fibers characterize painful phenotypes of diabetic neuropathy

Journal of Pain

Volumn 14, Issue 9, 2013, Pages 941-947

  Cheng, Hsinlin T ^a   Dauch, Jacqueline R ^a   Porzio, Michael T ^b   Yanik, Brandon M ^c   Hsieh, Wilson ^c   Smith, A Gordon ^b   Singleton, J Robinson ^b   Feldman, Eva L ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Diabetic pain; intraepidermal nerve fiber; peripheral neuropathy

Indexed keywords

CELL PROTEIN; NEUROMODULIN; PROTEIN GENE PRODUCT 9.5; SUBSTANCE P; TROPOMYOSIN RECEPTOR KINASE A; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DIABETIC NEUROPATHY; FEMALE; HUMAN; INTRAEPIDERMAL NERVE FIBER; MALE; NERVE FIBER; NERVE FIBER DEGENERATION; NERVE FIBER REGENERATION; NEUROPATHIC PAIN; NOCICEPTION; NON INSULIN DEPENDENT DIABETES MELLITUS; PHENOTYPE; PUNCH BIOPSY; SKIN BIOPSY;

DIABETIC PAIN; INTRAEPIDERMAL NERVE FIBER; PERIPHERAL NEUROPATHY;

AGED; AXONS; DIABETIC NEUROPATHIES; EPIDERMIS; FEMALE; GAP-43 PROTEIN; HUMANS; MALE; MIDDLE AGED; NERVE DEGENERATION; NERVE FIBERS; NEURALGIA; PAIN MEASUREMENT; RECEPTOR, TRKA; SUBSTANCE P; TRPV CATION CHANNELS;

EID: 84883788632     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2013.03.005     Document Type: Article

References (22)

1. S.T. Britland, R.J. Young, A.K. Sharma, and B.F. Clarke Association of painful and painless diabetic polyneuropathy with different patterns of nerve fiber degeneration and regeneration Diabetes 39 1990 898 908
2. H.T. Cheng, B. Callaghan, J.R. Dauch, and E.L. Feldman Cytoskeleton, axonal transport, and mechanisms of axonal neuropathy R.A. Nixon, A. Yuan, Cytoskeleton of the Nervous System 2011 Springer New York 657 678
3. H.T. Cheng, J.R. Dauch, J.M. Hayes, Y. Hong, and E.L. Feldman Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes J Neuropathol Exp Neurol 68 2009 1229 1243
4. H.T. Cheng, J.R. Dauch, J.M. Hayes, B.M. Yanik, and E.L. Feldman Nerve growth factor/p38 signaling increases intraepidermal nerve fiber densities in painful neuropathy of type 2 diabetes Neurobiol Dis 45 2012 280 287
5. J.A. Christianson, J.T. Riekhof, and D.E. Wright Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice Exp Neurol 179 2003 188 199
6. G.J. Ebenezer, J.C. McArthur, D. Thomas, B. Murinson, P. Hauer, M. Polydefkis, and J.W. Griffin Denervation of skin in neuropathies: The sequence of axonal and Schwann cell changes in skin biopsies Brain 130 2007 2703 2714
7. F. Fantini, and O. Johansson Expression of growth-associated protein 43 and nerve growth factor receptor in human skin: A comparative immunohistochemical investigation J Invest Dermatol 99 1992 734 742
8. C.H. Gibbons, J.W. Griffin, M. Polydefkis, I. Bonyhay, A. Brown, P.E. Hauer, and J.C. McArthur The utility of skin biopsy for prediction of progression in suspected small fiber neuropathy Neurology 66 2006 256 258
9. D.N. Herrmann, M.P. McDermott, D. Henderson, L. Chen, K. Akowuah, and G. Schifitto Epidermal nerve fiber density, axonal swellings and QST as predictors of HIV distal sensory neuropathy Muscle Nerve 29 2004 420 427
10. N.R. Holland, A. Stocks, P. Hauer, D.R. Cornblath, J.W. Griffin, and J.C. McArthur Intraepidermal nerve fiber density in patients with painful sensory neuropathy Neurology 48 1997 708 711
11. W.R. Kennedy, M. Nolano, G. Wendelschafer-Crabb, T.L. Johnson, and E. Tamura A skin blister method to study epidermal nerves in peripheral nerve disease Muscle Nerve 22 1999 360 371
12. G. Lauria, R. Lombardi, F. Camozzi, and G. Devigili Skin biopsy for the diagnosis of peripheral neuropathy Histopathology 54 2009 273 285
13. G. Lauria, M. Morbin, R. Lombardi, M. Borgna, G. Mazzoleni, A. Sghirlanzoni, and D. Pareyson Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies Neurology 61 2003 631 636
14. J.C. McArthur, E.A. Stocks, P. Hauer, D.R. Cornblath, and J.W. Griffin Epidermal nerve fiber density: Normative reference range and diagnostic efficiency Arch Neurol 55 1998 1513 1520
15. M. Polydefkis, P. Hauer, J.W. Griffin, and J.C. McArthur Skin biopsy as a tool to assess distal small fiber innervation in diabetic neuropathy Diabetes Technol Ther 3 2001 23 28
16. G. Said, G. Slama, and J. Selva Progressive centripetal degeneration of axons in small fibre diabetic polyneuropathy Brain 106 Pt 4 1983 791 807
17. C.T. Shun, Y.C. Chang, H.P. Wu, S.C. Hsieh, W.M. Lin, Y.H. Lin, T.Y. Tai, and S.T. Hsieh Skin denervation in type 2 diabetes: Correlations with diabetic duration and functional impairments Brain 127 2004 1593 1605
18. J.R. Singleton, B. Bixby, J.W. Russell, E.L. Feldman, A. Peltier, J. Goldstein, J. Howard, and A.G. Smith The Utah Early Neuropathy Scale: A sensitive clinical scale for early sensory predominant neuropathy J Peripher Nerv Syst 13 2008 218 227
19. L. Sorensen, L. Molyneaux, and D.K. Yue The level of small nerve fiber dysfunction does not predict pain in diabetic Neuropathy: A study using quantitative sensory testing Clin J Pain 22 2006 261 265
20. L. Sorensen, L. Molyneaux, and D.K. Yue The relationship among pain, sensory loss, and small nerve fibers in diabetes Diabetes Care 29 2006 883 887
21. A. Veves, M. Backonja, and R.A. Malik Painful diabetic neuropathy: Epidemiology, natural history, early diagnosis, and treatment options Pain Med 9 2008 660 674
22. H. Yasuda, M. Terada, K. Maeda, S. Kogawa, M. Sanada, M. Haneda, A. Kashiwagi, and R. Kikkawa Diabetic neuropathy and nerve regeneration Prog Neurobiol 69 2003 229 285