Ophthalmic markers of the diabetic polyneuropathy

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Abstract

In the article, a world literature analysis is presented on the relationship between structural and functional changes of the retina and of the optic nerve and the diabetic polyneuropathy severity degree. Diabetic polyneuropathy is one of the most common and severe complications of diabetes mellitus leading in many patients to ulcer formation and to foot amputation. Modern methods for neuropathy diagnosis either do not allow revealing early stage changes, or include invasive procedures. Ophthalmologists, involved in diabetic patients care, due to objective reasons focus on diabetic retinopathy. However, the evidence that the corneal nerves state is a marker of peripheral neuropathy suggests a new and very important role of the ophthalmologist in diabetic patient care. Several studies obtained promising results about structural and functional retinal changes could be found in diabetic patients before retinopathy start; this allows to suggest the neuropathy role at their origin.

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About the authors

Mariia I Krasavina

Federal Almazov North-West Medical Research Center

Email: mk702@yandex.ru
ophthalmologist

Sergey Yu Astakhov

First Pavlov State Medical University of St. Petersburg

Email: astakhov73@mail.ru
MD, PhD, Doc.Med.Sci., professor, head of the ophthalmology department

Fedor E Shadrichev

St. Petersburg territorial diabetology center

Email: shadrichev_dr@mail.ru
MD, candidate of medical science, head of the ophthalmology department

Nikita Yu Dal

eye clinic Zrenie

Email: ndahl@yandex.ru
MD, candidate of medical science, head of the eye clinic Zrenie

References

  1. Аветисов С.Э., Егорова Г.Б., Федоров А.А., и др. Конфокальная микроскопия роговицы. Сообщение 1. Особенности нормальной морфологической картины // Вестник офтальмологии. - 2008. - № 3. - С. 3-5. [Avetisov SE, Egorova GB, Fedorov AA, et al. Konfokal’naya mikroskopiya rogovitsy. Soobshchenie 1. Osobennosti normal’noi morfologicheskoi kartiny. Vestnik oftal’mologii. 2008;(3):3-5. (In Russ).]
  2. Красавина М.И., Астахов Ю.С., Шадричев Ф.Е. Может ли конфокальная микроскопия роговицы оценить повреждение нервных волокон у пациентов с диабетической полинейропатией? // Офтальмологические ведомости. - 2012. - Т. 5. - № 3. - С. 61-68. [Krasavina MI, Astakhov YS, Shadrichev FE. Mozhet li Konfokal’naya mikroskopiya rogovitsy otsenit’ povrezhdenie nervnykh volokon u patsientov s diabeticheskoi polineiropatiei? Ophtalmologic vedomosti. 2012;5(3);61-68. (In Russ).]
  3. Ткаченко Н.В., Астахов Ю.С. Диагностические возможности конфокальной микроскопии при исследовании поверхностных структур глазного яблока // Офтальмологические ведомости. - 2009. - Т 2. - № 1. - C. 82-89. [Tkachenko NV, Astakhov YS. Diagnosticheskie vozmozhnosti konfokal’noi mikroskopii pri issledovanii poverkhnostnykh struktur glaznogo yabloka. Ophtalmologic vedomosti. 2009;2(1):82-89. (In Russ).]
  4. Alberto M, Marina Z, Robert L. Nuclear apoptotic changes: An overview. J of Cellular Biochemistry. 2001;82(4):634-646. doi: 10.1002/jcb.1186.
  5. Algan M, Ziegler O, Gehin P, et al. Visual evoked potentials in diabetic patients. Diabetes Care. 1989;12(3):227-229. doi: 10.2337/diacare.12.3.227.
  6. Barber A, Lieth E, Khin S, et al. Neural apoptosis in the retina during experimental and human diabetes: Early onset and effect of insulin. J of Clin Invest. 1994;102:783-791.
  7. Barr E, Wong T, Tapp R, et al. Is peripheral neuropathy associated with retinopathy and albuminuria in individuals with impaired glucose metabolism. Diabetes Care. 2006;29(5):1114-1116. doi: 10.2337/diacare.2951114.
  8. Bearse J, Adams A, Han Y, et al. A multifocal electroretinogram model predicting the development of diabetic retinopathy. Progress in Retinal and Eye Research. 2006;25(5):425-448. doi: 10.1016/j.preteyeres.2006.07.001.
  9. Bell J, Feldon S. Retinal microangiopathy: Correlation of OCTOPUS perimetry with fluorescein angiography. Arch of Ophthalmology. 1984;102:1294-1298.
  10. Boulton A, Malik R, Arezzo J, et al. Diabetic somatic neuropathies. Diabetes Care. 2004;27(6):1458-1486. doi: 10.2337/diacare.27.6.1458.
  11. Bresnick G. Diabetic retinopathy viewed as a neurosensory disorder. Arch of Ophthalmology. 1986;104:989-990. doi: 10.1001/archopht.1986.01050190047037.
  12. Broadway D, Drance S, Parfitt C, et al. The ability of scanning laser ophthalmoscopy to identify various glaucomatous optic disk appearances. Am J of Ophthalmol. 1998;125(5):593-604. doi: 10.1016/s0002-9394(98)00002-6.
  13. Caputo S, Di Leo M, Falsini B, et al. Evidence for early impairment of macular function with pattern ERG in type I diabetic patients. Diabetes Care. 1990;13(4):412-418. doi: 10.2337/diacare.13.4.412.
  14. Chihara E, Matsuoka T, Ogura Y, et al. Retinal nerve fiber layer defect as an early manifestation of diabetic retinopathy. Ophthalmology. 1993;100(8):1147-1151. doi: 10.1016/s0161-6420(93)31513-7.
  15. Della Sala S, Bertoni G, Somazie L. Impaired contrast sensitivity in diabetic patients with and without retinopathy: a new technique for rapid assessment. Br J of Ophthalmol. 1985;69(2):136-142. doi: 10.1136/bjo.69.2.136
  16. Di Leo M, Caputo S, Falsini B, et al. Non-selective loss of contrast sensitivity in visual system testing in early type I diabetes. Diabetes Care. 1992;15(5):620-625. doi: 10.2337/diacare.15.5.620
  17. Di Leo M, Falsini B, Caputo S, et al.Spatial frequency-selective losses with pattern electroretinogram in type 1 (insulin-dependent) diabetic patients without retinopathy. Diabetologia. 1990;33(12):726-730. doi: 10.1007/bf00400342.
  18. Early Treatment of Diabetic Retinopathy Study Research Group. Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS Report Number 12. Ophthalmology. 1991;98:823-833.
  19. Ewing F, Deary I, McCrimmon R, et al. Effect of acute hypoglycemia on visual information processing in adults with type 1 diabetes mellitus. Physiology & Behavior. 1998;64(5):653-660. doi: 10.1016/s0031-9384(98)00120-6
  20. Gillies M, Su T, Stayt J, et al. Effect of high glucose on permeability of retinal capillary endothelium in vitro. Invest Ophthalmol and Vis Sci. 1997;38:635.
  21. Hardy K, Lipton J, Scase M, et al. Detection of colour vision abnormalities in uncomplicated type 1 diabetic patients with angiographically normal retinas. Br J of Ophthalmol. 1992;76(8):461-464. doi: 10.1136/bjo.76.8.461
  22. Henson D, North R. Dark adaptation in diabetes mellitus. Br J of Ophthalmol. 1979;63(8):539-541. doi: 10.1136/bjo.63.8.539.
  23. Hoyt W, Frisen L, Newman N, et al. Fundoscopy of nerve fiber layer defects in glaucoma. Invest Ophthalmol and Vis Sci. 1973;12:814-829.
  24. Jaffe G, Caprioli J. Optical coherence tomography to detect and manage retinal disease and glaucoma. Am J of Ophthalmol. 2004;137(1):156-169. doi: 10.1016/s0002-9394(03)00792-x.
  25. Katz J, Tielsch J, Quigley H, et al. Automated perimetry detects visual field loss before manual Goldmann perimetry. Ophthalmology. 1995;102(1):21-26. doi: 10.1016/s0161-6420(95)31060-3.
  26. Larsen M, Godt J, Larsen N, et al. Automated detection of fundus photographic red lesions in diabetic retinopathy. Invest Ophthalmol and Vis Sci. 2003;44(2):761-766. doi: 10.1167/iovs.02-0418
  27. Lobefalo L, Verrotti A, Mastropasqua L, et al. Flicker perimetry in diabetic children without retinopathy. Can J of Ophthalmol. 1997;32:324-328.
  28. Lopes de Faria J, Russ H, Costa V, et al. Retinal nerve fibre layer loss in patients with type 1 diabetes mellitus without retinopathy. Br J of Ophthalmol. 2002;86:725-728.
  29. Lovasik J, Spafford M. An electrophysiological investigation of visual function in juvenile insulin-dependent diabetes mellitus. Am J of Optometry and Physiological Optics. 1988;65:236-253. doi: 10.1097/00006324-198804000-00002.
  30. Malik R, Kallinikos P, Abbott C. Corneal confocal microscopy: a non-invasive surrogate of nerve fibre damage and repair in diabetic patients. Diabetologia. 2003;46:683-688.
  31. Mariani E, Moreo G, Colucci G, et al. Study of visual evoked potentials in diabetics without retinopathy: correlations with clinical findings and polyneuropathy. Acta Neurologica Scandinavica. 1990;81:337-340.
  32. Medeiros F, Sample P, Weinreb R, et al. Frequency doubling technology perimetry abnormalities as predictors of glaucomatous visual field loss. Am J of Ophthalmol. 2004;137(5):863-871. doi: 10.1016/j.ajo.2003.12.009.
  33. Mehra S, Tavakoli M, Kallinikos P, et al. Corneal confocal microscopy detects early nerve regeneration after pancreas transplantation in patients with type 1 diabetes. Diabetes Care. 2007;30:2608-2612. doi: 10.2337/dc07-0870.
  34. Menke M, Knecht P, Sturm V, et al. Reproducibility of nerve fiber layer thickness measurements using 3D Fourier-domain OCT. Invest Ophthalmol and Vis Sci. 2008;49(12):5386-5391. doi: 10.1167/iovs.07-1435.
  35. Merigan W, Byrne C, Maunsell J, et al. Does primate motion perception depend on the magnocellular pathway? The J of Neuroscience. 1991;11:3422-3429.
  36. Moavenshahidi A, Sampson G, Pritchard N, et al. Exploring retinal markers of diabetic neuropathy. Invest Ophthalmol and Vis Sci. 2010;51 E-abstract:2241. doi: 10.1111/j.1444-0938.2010.00491.x.
  37. Neckell A. Adaptometry in diabetic patients. Ophthalmologia. 2007; 51:95-97.
  38. Oliveira-Soto L, Efron N. Morphology of corneal nerves using confocal microscopy. Cornea. 2001;20(4):374-384. doi: 10.1097/00003226-200105000-00008.
  39. Oshitari T, Hanawa K, Adachi-Usami E, et al. Changes of macular and RNFL thicknesses measured by Stratus OCT in patients with early stage diabetes. Eye. 2009;23(4):884-889. doi: 10.1038/eye.2008.119
  40. Papakostopoulos D, Hart J, Corrall R, et al. The scotopic electroretinogram to blue flashes and pattern reversal visual evoked potentials in insulin dependent diabetes. Int J of Psychophysiology. 1996;21(1):33-43. doi: 10.1016/0167-8760(95)00040-2.
  41. Parravano M, Oddone F, Mineo D, et al. The role of Humphrey Matrix testing in the early diagnosis of retinopathy in type 1 diabetes. Br J of Ophthalmol. 2008;92:1656-1660.
  42. Pender P, Benson W, Compton H, et al. The effects of panretinal photocoagulation on dark adaptation in diabetics with proliferative retinopathy. Ophthalmology. 1981;88(7):635-638. doi: 10.1016/s0161-6420(81)34977-x.
  43. Quattrini C, Tavakoli M, Jeziorska M, et al. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes. 2007;56:2148-2154. doi: 10.2337/db07-0285.
  44. Remky A, Arend O, Hendricks S, et al. Short-wavelength automated perimetry and capillary density in early diabetic maculopathy. Invest Ophthalmol and Vis Sci. 2000;41:274-281.
  45. Roy M, Gunkel R, Podgor M, et al. Color vision defects in early diabetic retinopathy. Arch of Ophthalmology. 1986;104(2): 225-228. doi: 10.1001/archopht.1986.01050140079024.
  46. Shahidi A, Sampson G, Pritchard N, et al. Exploring retinal and functional markers of diabetic neuropathy. Clinical and Experimental Optometry. 2010;93(5):309-323. doi: 10.1111/j.1444-0938.2010.00491.x.
  47. Sharp P, Manivannan A, Vieira P, et al. Laser imaging of the retina. Br J of Ophthalmol. 1999;83:1241-1245.
  48. Skarf B. Retinal nerve fibre layer loss in diabetes mellitus without retinopathy. Br J of Ophthalmol. 2002;86 (7):709. doi: 10.1136/bjo.86.7.709.
  49. Sokol S, Moskowitz A, Skarf B, et al. Contrast sensitivity in diabetics with and without background retinopathy. Arch of Ophthalmology. 1985;103(1):51-54. doi: 10.1001/archopht.1985.01050010055018.
  50. Sommer A, Quigley H, Robin A, et al. Evaluation of nerve fiber layer assessment. Arch of Ophthalmology. 1984;102(12):1766-1771. doi: 10.1001/archopht.1984.01040031430017
  51. Stavrou E, Wood J. Central visual field changes using flicker perimetry in type 2 diabetes mellitus. Acta Ophthalmologica Scandinavica. 2005;83(5):574-580. doi: 10.1111/j.1600-0420.2005.00527.x.
  52. Stavrou E, Wood J. Letter contrast sensitivity changes in early diabetic retinopathy. Clinical and Experimental Optometry. 2003; 86(3):152-156. doi: 10.1111/j.1444-0938.2003.tb03097.x.
  53. Sugimoto M, Sasoh M, Ido M, et al. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica. 2005;219(6):379. doi: 10.1159/000088382.
  54. Tavakoli M, Kallinikos P, Efron N, et al. Corneal sensitivity is reduced and relates to the severity of neuropathy in patients with diabetes. Diabetes Care. 2007;30(7):1895-1897. doi: 10.2337/dc07-0175.
  55. Trick G, Trick L, Kilo C, et al. Visual field defects in patients with insulin-dependent and non-insulin-dependent diabetes. Ophthalmology. 1990;97(4):475-482. doi: 10.1016/s0161-6420(90)32557-5.
  56. Vujosevic S, Benetti E, Massignan F, et al. Screening for diabetic retinopathy: 1 and 3 nonmydriatic 45-degree digital fundus photographs vs 7 standard Early Treatment Diabetic Retinopathy Study fields. Am J of Ophthalmol. 2009;148(1):111-118. doi: 10.1016/j.ajo.2009.02.031.
  57. Wachtmeister L. Oscillatory potentials in the retina: what do they reveal? Progress in Retina and Eye Research. 1998;17(4):485-521. doi: 10.1016/s1350-9462(98)00006-8.
  58. Weinreb R, Bowd C, Zangwill L, et al. Glaucoma detection using scanning laser polarimetry with variable corneal polarization compensation. Arch of Ophthalmology. 2003;121(2):218-224. doi: 10.1001/archopht.121.2.218.
  59. Weymouth A, Vingrys A. Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Progress in Retinal and Eye Research. 2008;27(1):1-44. doi: 10.1016/j.preteyeres.2007.09.003.
  60. Yamazaki Y, Miyazawa T, Yamada H, et al. Retinal nerve fiber layer analysis by a computerized digital image analysis system. Jap J of Ophthalmol. 1990;34:174-180.
  61. Yoshiaki S, Yong L, Marcus A, et al. Assessment of early retinal changes in diabetes using a new multifocal ERG protocol. Br J of Ophthalmol. 2001;85(4):414. doi: 10.1136/bjo.85.4.414.

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Copyright (c) 2016 Krasavina M.I., Astakhov S.Y., Shadrichev F.E., Dal N.Y.

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