Assessing corneal nerve structure and function in diabetic neuropathy

Clinical and Experimental Optometry

Volumn 95, Issue 3, 2012, Pages 338-347

  Tavakoli, Mitra ^a   Petropoulos, Ioannis N ^a   Malik, Rayaz A ^a  

^a MANCHESTER ROYAL INFIRMARY   (United Kingdom)

Author keywords

Cornea; Corneal nerves; Diabetes; Diabetic neuropathy; In vivo corneal confocal microscopy (IVCCM)

Indexed keywords

ADULT; AGE; AGED; CONFOCAL MICROSCOPY; CORNEA; DIABETIC NEUROPATHY; HUMAN; INNERVATION; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NERVE; REVIEW;

ADULT; AGE FACTORS; AGED; CORNEA; DIABETIC NEUROPATHIES; HUMANS; MICROSCOPY, CONFOCAL; MIDDLE AGED; PERIPHERAL NERVES;

EID: 84861213330     PISSN: 08164622     EISSN: 14440938     Source Type: Journal    
DOI: 10.1111/j.1444-0938.2012.00743.x     Document Type: Review

References (84)

1. Boulton AJM, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care 2004; 27: 1458-1486.
2. Abbott CA, Vileikyte L, Williamson S, Carrington AL, Boulton AJ. Multicenter study of the incidence of and predictive risk factors for diabetic neuropathic foot ulceration. Diabetes Care 1998; 21: 1071-1075.
3. Mojaddidi M, Quattrini C, Tavakoli M, Malik R. Recent developments in the assessment of efficacy in clinical trials of diabetic neuropathy. Curr Diab Rep 2005; 5: 417-422.
4. Hossain P, Sachdev A, Malik RA. Early detection of diabetic peripheral neuropathy with corneal confocal microscopy. Lancet 2005; 366: 1340-1343.
5. Quattrini C, Tavakoli M, Jeziorska M, Kallinikos P, Tesfaye S, Finnigan J, Marshall A etal. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 2007; 56: 2148-2154.
6. Boucek P, Havrdova T, Voska L, Lodererova A, Saudek F, Lipar K, Janousek L etal. Severe depletion of intraepidermal nerve fibers in skin biopsies of pancreas transplant recipients. Transplant Proc 2005; 37: 3574-3575.
7. Mehra S, Tavakoli M, Kallinikos PA, Efron N, Boulton AJM, Augustine T, Malik RA. Corneal confocal microscopy detects early nerve regeneration after pancreas transplantation in patients with type 1 diabetes. Diabetes Care 2007; 30: 2608-2612.
8. Tavakoli M, Kallinikos PA, Efron N, Boulton AJ, Malik RA. Corneal sensitivity is reduced and relates to the severity of neuropathy in patients with diabetes. Diabetes Care 2007; 30: 1895-1897.
9. Sorensen L, Molyneaux L, Yue DK. The relationship among pain, sensory loss, and small nerve fibers in diabetes. Diabetes Care 2006; 29: 883-887.
10. Tavakoli M, Marshall A, Pitceathly R, Fadavi H, Gow D, Roberts ME, Efron N etal. Corneal confocal microscopy: a novel means to detect nerve fibre damage in idiopathic small fibre neuropathy. Exp Neurol 2010; 223: 245-250.
11. Tavakoli M, Marshall A, Thompson L, Kenny M, Waldek S, Efron N, Malik RA. Corneal confocal microscopy: a novel non-invasive means to diagnose neuropathy in patients with Fabry disease. Muscle Nerve 2009; 40: 976-984.
12. Müller LJ, Marfurt CF, Kruse F, Tervo TMT. Corneal nerves: structure, contents and function. Exp Eye Res 2003; 76: 521-542.
13. Gallar J, Acosta MC, Moilanen JA, Holopainen JM, Belmonte C, Tervo TM. Recovery of corneal sensitivity to mechanical and chemical stimulation after laser in situ keratomileusis. J Refract Surg 2004; 20: 229-235.
14. Marfurt CF, Murphy CJ, Florczak JL. Morphology and neurochemistry of canine corneal innervation. Invest Ophthalmol Vis Sci 2001; 42: 2242-2251.
15. Guthoff RF, Wienss H, Hahnel C, Wree A. Epithelial innervation of human cornea: a three-dimensional study using confocal laser scanning fluorescence microscopy. Cornea 2005; 24: 608-613.
16. Beuerman RW, Pedroza L. Ultrastructure of the human cornea. Microsc Res Tech 1996; 33: 320-335.
17. Müller LJ, Pels L, Vrensen GF. Ultrastructural organization of human corneal nerves. Invest Ophthalmol Vis Sci 1996; 37: 476-488.
18. Jones MA, Marfurt CF. Peptidergic innervation of the rat cornea. Exp Eye Res 1998; 66: 421-435.
19. Müller LJ, Vrensen GF, Pels L, Cardozo BN, Willekens B. Architecture of human corneal nerves. Invest Ophthalmol Vis Sci 1997; 38: 985-994.
20. Beckers H, Klooster J, Vrensen G, Lamers W. Sympathetic innervation of the rat's eye and peripheral ganglia: an electron microscopic autoradiographic tracing study. Graef Arch Clin and Exp Ophthalmol 1994; 232: 57-65.
21. Marfurt CF, Cox J, Deek S, Dvorscak L. Anatomy of the human corneal innervation. Exp Eye Res 2010; 90: 478-492.
22. Oliveira-Soto L, Efron N. Morphology of corneal nerves using confocal microscopy. Cornea 2001; 20: 374-384.
23. Patel DV, McGhee CNJ. Mapping of the normal human corneal sub-basal nerve plexus by in vivo laser scanning confocal microscopy. Invest Ophthalmol Vis Sci 2005; 46: 4485-4488.
24. Patel DV, McGhee CNJ. Mapping the corneal sub-basal nerve plexus in keratoconus by in vivo laser scanning confocal microscopy. Invest Ophthalmol Vis Sci 2006; 47: 1348-1351.
25. Møller-Pedersen T, Li HF, Petroll WM, Cavanagh HD, Jester JV. Confocal microscopic characterization of wound repair after photorefractive keratectomy. Invest Ophthalmol Vis Sci 1998; 39: 487-501.
26. Yokogawa H, Kobayashi A, Sugiyama K. Mapping of normal corneal K-structures by in vivo laser confocal microscopy. Cornea 2008; 27: 879-883.
27. Mannion LS, Tromans C, O'Donnell C. Corneal nerve structure and function in keratoconus: a case report. Eye Contact Lens 2007; 33: 106-108.
28. Belmonte C, Carmen Acosta M, Gallar J. Neural basis of sensation in intact and injured corneas. Exp Eye Res 2004; 78: 513-525.
29. Ueda S, Rao GN, LoCascio JA, del Cerro M, Aquavella JV. Corneal and conjunctival changes in congenital erythropoietic porphyria. Cornea 1989; 8: 286-294.
30. Stachs O, Zhivov A, Kraak R, Stave J, Guthoff R. In vivo three-dimensional confocal laser scanning microscopy of the epithelial nerve structure in the human cornea. Graef Arch Clinical Exp Ophthalmol 2007; 245: 569-575.
31. Henderson L, Bond D, Simpson T. The association between eye color and corneal sensitivity measured using a Belmonte esthesiometer. Optom Vis Sci 2005; 82: 629-632.
32. Millodot M, Owens H. The influence of age on the fragility of the cornea. Acta Ophthalmol 1984; 62: 819-824.
33. Murphy PJ, Patel S, Marshall J. The effect of long-term, daily contact lens wear on corneal sensitivity. Cornea 2001; 20: 264-269.
34. Darwish T, Brahma A, Efron N, O'Donnell C. Subbasal nerve regeneration after penetrating keratoplasty. Cornea 2007; 26: 935-940.
35. Darwish T, Brahma A, O'Donnell C, Efron N. Subbasal nerve fiber regeneration after LASIK and LASEK assessed by noncontact esthesiometry and in vivo confocal microscopy: prospective study. J Cataract Refract Surg 2007; 33: 1515-1521.
36. Pritchard N, Edwards K, Vagenas D, Shahidi AM, Sampson GP, Russell AW, Malik RA etal. Corneal sensitivity as an ophthalmic marker of diabetic neuropathy. Optom Vis Sci 2010; 87: 1003-1008.
37. Roszkowska AM, Colosi P, Ferreri FM, Galasso S. Age-related modifications of corneal sensitivity. Opthalmologica 2004; 218: 350-355.
38. Millodot M. The influence of age on the sensitivity of the cornea. Invest Ophthalmol Vis Sci 1977; 16: 240-242.
39. Grupcheva CN, Wong T, Riley AF, McGhee CNJ. Assessing the sub-basal nerve plexus of the living healthy human cornea by in vivo confocal microscopy. Clin Experiment Ophthalmol 2002; 30: 187-190.
40. Patel DV, Tavakoli M, Craig JP, Efron N, McGhee CNJ. Corneal sensitivity and slit scanning in vivo confocal microscopy of the sub-basal nerve plexus of the normal central and peripheral human cornea. Cornea 2009; 28: 735-740.
41. Erie JC, McLaren JW, Hodge DO, Bourne WM. The effect of age on the corneal subbasal nerve plexus. Cornea 2005; 24: 705-709.
42. Niederer RL, Perumal D, Sherwin T, McGhee CNJ. Age-related differences in the normal human cornea: a laser scanning in vivo confocal microscopy study. Br J Ophthalmol 2007; 91: 1165-1169.
43. He J, Bazan NG, Bazan HEP. Mapping the entire human corneal nerve architecture. Exp Eye Res 2010; 91: 513-523.
44. Pritchard N, Edwards K, Shahidi AM, Sampson GP, Russell AW, Malik RA, Efron N. Corneal markers of diabetic neuropathy. Ocul Surf 2011; 9: 17-28.
45. Zhivov A, Blum M, Guthoff R, Stachs O. Real-time mapping of the subepithelial nerve plexus by in vivo confocal laser scanning microscopy. Br J Ophthalmol 2010; 94: 1133-1135.
46. Chang P-Y, Carrel H, Huang J-S, Wang IJ, Hou Y-C, Chen W-L, Wang J-Y etal. Decreased density of corneal basal epithelium and subbasal corneal nerve bundle changes in patients with diabetic retinopathy. Am J Ophthalmol 2006; 142: 488-490.
47. Malik RA, Kallinikos P, Abbott CA, van Schie CHM, Morgan P, Efron N, Boulton AJM. Corneal confocal microscopy: a non-invasive surrogate of nerve fibre damage and repair in diabetic patients. Diabetologia 2003; 46: 683-688.
48. Tavakoli M, Quattrini C, Abbott C, Kallinikos P, Marshall A, Finnigan J, Morgan P etal. Corneal confocal microscopy. A novel non-invasive test to diagnose and stratify the severity of human diabetic neuropathy. Diabetes Care 2010; 33: 1792-1797.
49. Messmer E, Schmid-Tannwald C, Zapp D, Kampik A. In vivo confocal microscopy of corneal small fiber damage in diabetes mellitus. Graef Arch Clin Exp Ophthalmol 2010; 248: 1307-1312.
50. Midena E, Brugin E, Ghirlando A, Sommavilla M, Avogaro A. Corneal diabetic neuropathy: a confocal microscopy study. J Refract Surg 2006; 25: 1047.
51. Dabbah MA, Graham J, Petropoulos IN, Tavakoli M, Malik RA. Automatic analysis of diabetic peripheral neuropathy using multi-scale quantitative morphology of nerve fibres in corneal confocal microscopy imaging. Med Image Anal 2011; 15: 738-747.
52. Scarpa F, Grisan E, Ruggeri A. Automatic recognition of corneal nerve structures in images from confocal microscopy. Invest Ophthalmol Vis Sci 2008; 49: 4801-4807.
53. Hosal BM, Ornek N, Zilelioglu G, Elhan AH. Morphology of corneal nerves and corneal sensation in dry eye: a preliminary study. Eye 2004; 19: 1276-1279.
54. Simo Mannion L, Tromans C, O'Donnell C. An evaluation of corneal nerve morphology and function in moderate keratoconus. Cont Lens Anterior Eye 2005; 28: 185-192.
55. Patel DV, McGhee CNJ. In vivo confocal microscopy of corneal stromal nerves in patients with peripheral neuropathy. Arch Neurol 2009; 66: 1179-1180.
56. Al-Aqaba MA, Alomar T, Miri A, Fares U, Otri AM, Dua HS. Ex vivo confocal microscopy of human corneal nerves. Br J Ophthalmol 2010; 94: 1251-1257.
57. Allen VD, Malinovsky V. Management of neurotrophic keratopathy. Cont Lens Anterior Eye 2003; 26: 161-165.
58. Yamada J, Reza Dana M, Sotozono C, Kinoshita S. Local suppression of IL-1 by receptor antagonist in the rat model of corneal alkali injury. Exp Eye Res 2003; 76: 161-167.
59. Chikama T, Fukuda K, Morishige N, Nishida T. Treatment of neurotrophic keratopathy with substance-P-derived peptide (FGLM) and insulin-like growth factor I. Lancet 1998; 351: 1783-1784.
60. Rosenberg ME, Tervo TMT, Immonen IJ, Müller LJ, Grönhagen-Riska C, Vesaluoma MH. Corneal structure and sensitivity in type 1 diabetes mellitus. Invest Ophthalmol Vis Sci 2000; 41: 2915-2921.
61. Fraunfelder FW, Rich LF. Laser-assisted in situ keratomileusis complications in diabetes mellitus. Cornea 2002; 21: 246-248.
62. Rosenberg ME, Tervo TMT, Müller LJ, Moilanen JAO, Vesaluoma MH. In vivo confocal microscopy after herpes keratitis. Cornea 2002; 21: 265-269.
63. Su P-Y, Hu F-R, Chen Y-M, Han J-H, Chen W-L. Dendritiform cells found in central cornea by in-vivo confocal microscopy in a patient with mixed bacterial keratitis. Ocul Immunol Inflamm 2006; 14: 241-244.
64. Tavakoli M, Boulton AJM, Efron N, Malik RA. Increased Langerhan cell density and corneal nerve damage in diabetic patients: role of immune mechanisms in human diabetic neuropathy. Cont Lens Anterior Eye 2011; 34: 7-11.
65. Zhivov A, Stave J, Vollmar B, Guthoff R. In vivo confocal microscopic evaluation of Langerhans cell density and distribution in the normal human corneal epithelium. Graef Arch Clin Exp Ophthalmol 2005; 243: 1056-1061.
66. Zhivov A, Stave J, Vollmar B, Guthoff R. In vivo confocal microscopic evaluation of Langerhans cell density and distribution in the corneal epithelium of healthy volunteers and contact lens wearers. Cornea 2007; 26: 47-54.
67. Mastropasqua L, Nubile M, Lanzini M, Carpineto P, Ciancaglini M, Pannellini T, Di Nicola M etal. Epithelial dendritic cell distribution in normal and inflamed human cornea: in vivo confocal microscopy study. Am J Ophthalmol 2006; 142: 736-744.
68. Benítez-del-Castillo JM, Acosta MC, Wassfi MA, Díaz-Valle D, Gegúndez JA, Fernandez C, García-Sánchez J. Relation between corneal innervation with confocal microscopy and corneal sensitivity with noncontact esthesiometry in patients with dry eye. Invest Ophthalmol Vis Sci 2007; 48: 173-181.
69. Gemignani F, Ferrari G, Vitetta F, Giovanelli M, Macaluso C, Marbini A. Non-length-dependent small fibre neuropathy. Confocal microscopy study of the corneal innervation. J Neurol Neurosurg Psychiatry 2010; 81: 731-733.
70. Tuisku IS, Konttinen YT, Konttinen LM, Tervo TM. Alterations in corneal sensitivity and nerve morphology in patients with primary Sjögren's syndrome. Exp Eye Res 2008; 86: 879-885.
71. Mimura T, Amano S, Fukuoka S, Honda N, Arita R, Ochiai M, Yanagisawa M etal. In vivo confocal microscopy of hereditary sensory and autonomic neuropathy. Curr Eye Res 2008; 33: 940-945.
72. Lalive PH, Truffert A, Magistris MR, Landis T, Dosso A. Peripheral autoimmune neuropathy assessed using corneal in vivo confocal microscopy. Arch Neurol 2009; 66: 403-405.
73. Ferrari G, Gemignani F, Macaluso C. Chemotherapy-associated peripheral sensory neuropathy assessed using in vivo corneal confocal microscopy. Arch Neurol 2010; 67: 364-365.
74. Hyndiuk RA, Kazarian EL, Schultz RO, Seideman S. Neurotrophic corneal ulcers in diabetes mellitus. Arch Ophthalmol 1977; 95: 2193-2196.
75. Ishida N, Rao GN, del Cerro M, Aquavella JV. Corneal nerve alterations in diabetes mellitus. Arch Ophthalmol 1984; 102: 1380-1384.
76. Kim HC, Cho YJ, Ahn CW, Park KS, Kim JC, Nam JS, Im YS etal. Nerve growth factor and expression of its receptors in patients with diabetic neuropathy. Diabet Med 2009; 26: 1228-1234.
77. Efron N, Edwards K, Roper N, Pritchard N, Sampson GP, Shahidi AM, Vagenas D etal. Repeatability of measuring corneal subbasal nerve fiber length in individuals with type 2 diabetes. Eye Contact Lens 2010; 36: 245-248.
78. Schwartz DE. Corneal sensitivity in diabetics. Arch Ophthalmol 1974; 91: 174-178.
79. Rogell GD. Corneal hypesthesia and retinopathy in diabetes mellitus. Ophthalmology 1980; 87: 229-233.
80. Daubs JG. Diabetes screening with corneal aesthesiometer. Aust J Optom 1975; 58: 132-135.
81. Nielsen NV. Corneal sensitivity and vibratory perception in diabetes mellitus. Acta Ophthalmol 1978; 56: 406-411.
82. Murphy PJ, Patel S, Kong N, Ryder REJ, Marshall J. Non-invasive assessment of corneal sensitivity in young and elderly diabetic and nondiabetic subjects. Invest Ophthalmol Vis Sci 2004; 45: 1737-1742.
83. Nuho A, Subekti I, Ismail D, Sitompul R. Correlation of neuropathy with corneal sensitivity and lacrimal gland secretion in type 2 diabetes mellitus patient. Acta Med Indones 2004; 36: 130-135.
84. Neira-Zalentein W, Holopainen JM, Tervo TMT, Borrás F, Acosta MC, Belmonte C, Gallar J. Corneal sensitivity in diabetic patients subjected to retinal laser photocoagulation. Invest Ophthalmol Vis Sci 2011; 52: 6043-6049.