Retinal Sensitivity in Patients with Type I Diabetes without Retinopathy or with Minor Retinal Changes

I. Pinilla; A. Sanchez-Cano; A. Ferreras; J. Acha; D. Pérez-García; J. Ibañez-Alperte; E. Abecia

doi:10.1055/s-0042-111045

Experimental and Clinical Endocrinology & Diabetes, Inhaltsverzeichnis

Exp Clin Endocrinol Diabetes 2016; 124(10): 613-617
DOI: 10.1055/s-0042-111045

Article

Retinal Sensitivity in Patients with Type I Diabetes without Retinopathy or with Minor Retinal Changes

I. Pinilla

¹Department of Ophthalmology, Lozano Blesa University Hospital, Zaragoza, Spain

²Department of Surgery, Gynecology and Obstetrics, University of Zaragoza, Zaragoza, Spain

³Aragon Institute for Health Research, Zaragoza, Spain

,

A. Sanchez-Cano

³Aragon Institute for Health Research, Zaragoza, Spain

⁴Department of Applied Physics, University of Zaragoza, Zaragoza, Spain

,

A. Ferreras

²Department of Surgery, Gynecology and Obstetrics, University of Zaragoza, Zaragoza, Spain

³Aragon Institute for Health Research, Zaragoza, Spain

⁵Department of Ophthalmology, Miguel Servet University Hospital, Zaragoza, Spain

,

J. Acha

⁶Department of Endocrinology, Miguel Servet University Hospital, Zaragoza, Spain

,

D. Pérez-García

¹Department of Ophthalmology, Lozano Blesa University Hospital, Zaragoza, Spain

³Aragon Institute for Health Research, Zaragoza, Spain

,

J. Ibañez-Alperte

¹Department of Ophthalmology, Lozano Blesa University Hospital, Zaragoza, Spain

³Aragon Institute for Health Research, Zaragoza, Spain

,

E. Abecia

²Department of Surgery, Gynecology and Obstetrics, University of Zaragoza, Zaragoza, Spain

³Aragon Institute for Health Research, Zaragoza, Spain

⁵Department of Ophthalmology, Miguel Servet University Hospital, Zaragoza, Spain

› Institutsangaben

Abstract

Objective: To evaluate the ability of short-wavelength automated perimetry (SWAP) for the detection of visual impairment in patients with type I diabetes without retinopathy or with minor retinal vascular changes.

Design: Comparative cross-sectional study.

Participants: 30 eyes of 30 healthy subjects and 73 eyes of 73 patients with type I diabetes mellitus were studied.

Methods: Ophthalmic examination of diabetic patients showed no retinopathy or minimal changes (less than 5 microaneurisms in each eye) with no previous laser treatment. All patients were examined by means of the SWAP 24-2 strategy. Mean Deviation (MD) and Pattern Standard Deviation (PSD) were compared between both groups.

Results: There were differences in the clusters of altered points between both groups (p=0.004). SWAP MD was lower in the diabetic group than in the controls (−2.89 dB vs. −0.20 dB, p<0.001). SWAP PSD also differed between both groups (2.50 dB in control group, 3.12 dB in the diabetic group, p=0.003). In the diabetic group, mean period from the onset of diabetes was 12.6±6.7 years and minimal vascular changes were observed in the retina of 18 eyes (24.7%), while 55 had no lesions (75.3%). No differences in SWAP changes were found between patients without and with minimal diabetic retinopathy.

Conclusions: Retinal sensitivity assessed by SWAP is depressed in patients with type I diabetes regardless of the presence of retinal vascular changes.

Key words

diabetes - retinopathy - microaneurisms - short-wavelength automated perimetry - visual field

Volltext

Referenzen

References
1 Ewing FME, Deary IJ, Strachan MWJ et al. Seeing beyond retinopathy in diabetes: Electrophysiological and psychophysical abnormalities and alterations in vision. Endocr Rev 1998; 19: 462-476
2 della Sala S, Bertoni G, Somazzi L et al. Impaired contrast sensitivity in diabetic patients with and without retinopathy: A new technique for rapid assessment. Br J Ophthalmol 1985; 69: 136-142
3 Sokol S, Moskowitz A, Skarf B et al. Contrast sensitivity in diabetics with and without background retinopathy. Arch Ophthalmol 1985; 103: 51-54
4 Ismail GM, Whitaker D. Early detection of changes in visual function in diabetes mellitus. Ophthalmic Physiol Opt 1998; 18: 3-12
5 Frost-Larsen K, Sandahl Christiansen J, Parving H. The effect of strict short-term metabolic control on retinal nervous system abnormalities in newly diagnosed Type 1 (insulin-dependent) diabetic patients. Diabetologia 1983; 24: 207-209
6 Lovasik JV, Spafford MM. An electrophysiological investigation of visual function in juvenile insulin-dependent diabetes mellitus. Am J Optom Physiol Opt 1988; 65: 236-253
7 Di Leo MAS, 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: 726-730
8 Greco AV, Di Leo MAS, Caputo S et al. Early selective neuroretinal disorder in prepubertal type 1 (insulin-dependent) diabetic children without microvascular abnormalities. Acta Diabetol 1994; 31: 98-102
9 Kurtenbach A, Langrova H, Zrenner E. Multifocal oscillatory potentials in Type 1 diabetes without retinopathy. Invest Ophthalmol Vis Sci 2000; 41: 3234-3241
10 Bearse Jr MA, Han Y, Schneck ME et al. Retinal Function in Normal and Diabetic Eyes Mapped with the Slow Flash Multifocal Electroretinogram. Invest Ophthalmol Vis Sci 2004; 45: 296-304
11 Puvanendran K, Devathasan G, Wong PK. Visual evoked responses in diabetes. J Neurol Neurosurg Psychiatry 1983; 46: 643-647
12 Anastasi M, Lauricella M, Giordano C et al. Visual evoked potentials in insulin-dependent diabetics. Acta Diabetol Lat 1985; 22: 343-349
13 Pozzessere G, Rizzo PA, Valle E et al. Early detection of neurological involvement in IDDM and NIDDM. Multimodal evoked potentials versus metabolic control. Diabetes Care 1988; 11: 473-480
14 Yaltkaya K, Balkan S, Baysal AI. Visual evoked potentials in diabetes mellitus. Acta Neurol Scand 1988; 77: 239-241
15 Mariani E, Moreo G, Colucci GB. Study of visual evoked potentials in diabetics without retinopathy: Correlations with clinical findings and polyneuropathy. Acta Neurol Scand 1990; 81: 337-340
16 Martinelli V, Filippi IM, Meschi F et al. Electrophysiological study of optic pathways in insulin dependent diabetes mellitus. Clinical Vision Sciences 1991; 6: 437-443
17 Pozzessere G, Valle E, De Crignis S et al. Abnormalities of cognitive functions in IDDM revealed by P300 event-related potential analysis. Comparison with short-latency evoked potentials and psychometric tests. Diabetes 1991; 40: 952-958
18 Uccioli L, Parisi V, Monticone G et al. Electrophysiological assessment of visual function in newly diagnosed IDDM patients. Diabetologia 1995; 38: 804-808
19 Chihara E, Matsuoka T, Ogura Y et al. Retinal nerve fiber layer defect as an early manifestation of diabetic retinopathy. Ophthalmology 1993; 100: 1147-1151
20 Abrishami M, Daneshvar R, Yaghubi Z. Short-wavelength automated perimetry in type I diabetic patients without retinal involvement: A test modification to decrease test duration. Eur J Ophthalmol 2012; 22: 203-209
21 Pinilla I, Ferreras A, Idoipe M et al. Changes in frequency-doubling perimetry in patients with type I diabetes prior to retinopathy. Biomed Res Int 2013; 2013 341269
22 Kinnear PR, Aspinall PA, Lakowski R. The diabetic eye and colour vision. Trans Ophthalmol Soc U K 1972; 92: 69-78
23 Antonetti DA, Barber AJ, Bronson SK et al. Diabetic retinopathy: Seeing beyond glucose-induced microvascular disease. Diabetes 2006; 55: 2401-2411
24 Barber AJ. A new view of diabetic retinopathy: A neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27: 283-290
25 Villarroel M, Ciudin A, Hernández C et al. Neurodegeneration: An early event of diabetic retinopathy. World J Diabetes 2010; 1: 57-64
26 Barber AJ, Lieth E, Khin SA et al. Neural apoptosis in the retina during experimental and human diabetes: Early onset and effect of insulin. J Clin Invest 1998; 102: 783-791
27 Martin PM, Roon P, Van Ells TK et al. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci 2004; 45: 3330-3336
28 Park S, Park J, Park S et al. Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia 2003; 46: 1260-1268
29 Aizu Y, Oyanagi K, Hu J et al. Degeneration of retinal neuronal processes and pigment epithelium in the early stage of the streptozotocin-diabetic rats. Neuropathology 2002; 22: 161-170
30 Gastinger MJ, Singh RSJ, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas. Invest Ophthalmol Vis Sci 2006; 47: 3143-3150
31 Mizutani M, Kern TS, Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest 1996; 97: 2883-2890
32 Lorenzi M, Gerhardinger C. Early cellular and molecular changes induced by diabetes in the retina. Diabetologia 2001; 44: 791-804
33 Daley ML, Watzke RC, Riddle MC. Early loss of blue-sensitive color vision in patients with type I diabetes. Diabetes Care 1987; 10: 777-7781
34 Greenstein VC, Hood DC, Ritch R et al. S (blue) cone pathway vulnerability in retinitis pigmentosa, diabetes and glaucoma. Invest Ophthalmol Vis Sci 1989; 30: 1732-1737
35 Greenstein V, Sarter B, Hood D et al. Hue discrimination and S-cone pathway sensitivity in early diabetic retinopathy. Invest Ophthalmol Vis Sci 1990; 31: 1008-1014
36 Hardy KJ, Fisher C, Heath P et al. Comparison of colour discrimination and electroretinography in evaluation of visual pathway dysfunction in aretinopathic IDDM patients. Br J Ophthalmol 1995; 79: 35-37
37 Phipps JA, Fletcher EL, Vingrys AJ. Paired-flash identification of rod and cone dysfunction in the diabetic rat. Invest Ophthalmol Vis Sci 2004; 45: 4592-4600
38 Yamamoto S, Kamiyama M, Nitta K et al. Selective reduction of the S cone electroretinogram in diabetes. Br J Ophthalmol 1996; 80: 973-975
39 Yamamoto S, Takeuchi S, Kamiyama M. The short wavelength-sensitive cone electroretinogram in diabetes: Relationship to systemic factors. Doc Ophthalmol 1997; 94: 193-200
40 Semeran K, Pawlowski P, Lisowski L et al. Plasma levels of il-17, VEGF, and adrenomedullin and s-cone dysfunction of the retina in children and adolescents without signs of retinopathy and with varied duration of diabetes. Mediators Inflamm 2013; 2013: 274726
41 Cho N, Poulsen GL, Ver Hoeve JN et al. Selective loss of S-cones in diabetic retinopathy. Arch Ophthalmol 2000; 118: 1393-1400
42 Remky A, Weber A, Hendricks S et al. Short-wavelength automated perimetry in patients with diabetes mellitus without macular edema. Graefes Arch Clin Exp Ophthalmol 2003; 241: 468-471
43 Nomura R, Terasaki H, Hirose H et al. Blue-on-yellow perimetry to evaluate S cone sensitivity in diabetics. Ophthalmic Res 2000; 32: 69-72
44 Afrashi F, Erakgün T, Köse S et al. Blue-on-yellow perimetry versus achromatic perimetry in type 1 diabetes patients without retinopathy. Diabetes Res Clin Pract 2003; 61: 7-11
45 Zico OA, El-Shazly AA, Ahmed EEA. Short wavelength automated perimetry can detect visual field changes in diabetic patients without retinopathy. Indian J Ophthalmol 2014; 62: 383-387
46 Han Y, Adams AJ, Bearse Jr MA et al. Multifocal electroretinogram and short-wavelength automated perimetry measures in diabetic eyes with little or no retinopathy. Arch Ophthalmol 2004; 122: 1809-1815
47 Chylack Jr., LT, Wolfe JK et al. The Lens Opacities Classification System III. Arch Ophthalmol 1993; 111: 831-836
48 Fogagnolo P, Rossetti L, Ranno S et al. Short-wavelength automated perimetry and frequency-doubling technology perimetry in glaucoma. Prog Brain Res 2008; 173: 101-124
49 Polo V, Larrosa JM, Pinilla I et al. Optimum criteria for short-wavelength automated perimetry. Ophthalmology 2001; 108: 285-289
50 Patz A, Rice TA, Murphy RP. Photocoagulation for diabetic macular edema. Arch Ophthalmol 1985; 103: 1796-1806
51 Heron G, Adams AJ, Husted R. Central visual fields for short wavelength sensitive pathways in glaucoma and ocular hypertension. Invest Ophthalmol Vis Sci 1988; 29: 64-72
52 Hart Jr. WM, Silverman SE, Trick GL et al. Glaucomatous visual field damage. Luminance and color-contrast sensitivities. Invest Ophthalmol Vis Sci 1990; 31: 359-367
53 Sample PA, Weinreb RN. Color perimetry for assessment of primary open-angle glaucoma. Invest Ophthalmol Vis Sci 1990; 31: 1869-1875
54 Sample PA, Weinreb RN. Progressive color visual field loss in glaucoma. Invest Ophthalmol Vis Sci 1992; 33: 2068-2071
55 Sample PA, Taylor JDN, Martinez GA et al. Short-wavelength color visual fields in glaucoma suspects at risk. Am J Ophthalmol 1993; 115: 225-233
56 Ferreras A, Polo V, Larrosa JM et al. Can frequency-doubling technology and short-wavelength automated perimetries detect visual field defects before standard automated perimetry in patients with preperimetric glaucoma?. J Glaucoma 2007; 16: 372-383
57 Teesalu P, Airaksinen PJ, Tuulonen A. Blue-on-yellow visual field and retinal nerve fiber layer in ocular hypertension and glaucoma. Ophthalmology 1998; 105: 2077-2081
58 Yücel YH, Zhang Q, Weinreb RN et al. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res 2003; 22: 465-481
59 Sample PA, Madrid ME, Weinreb RN. Evidence for a variety of functional defects in glaucoma-suspect eyes. J Glaucoma 1994; 3 (Suppl. 01) S5-S18
60 Johnson CA. Selective versus nonselective losses in glaucoma. J Glaucoma 1994; 3 (Suppl. 01) S32-S44
61 Wild JM. Short wavelength automated perimetry. Acta Ophthalmol Scand 2001; 79: 546-559
62 Blumenthal EZ, Sample PA, Berry CC et al. Evaluating several sources of variability for standard and SWAP visual fields in glaucoma patients, suspects, and normals. Ophthalmology 2003; 110: 1895-1902
63 Hutchings N, Hosking SL, Wild JM et al. Long-term fluctuation in short-wavelength automated perimetry in glaucoma suspects and glaucoma patients. Invest Ophthalmol Vis Sci 2001; 42: 2332-2337
64 Kim YY, Kim JS, Shin DH et al. Effect of cataract extraction on blue-on-yellow visual field. Am J Ophthalmol 2001; 132: 217-220
65 Kurtenbach A, Schiefer U, Neu A et al. Preretinopic changes in the colour vision of juvenile diabetics. Br J Ophthalmol 1999; 83: 43-46
66 Henson DB, North RV. Dark adaptation in diabetes mellitus. Br J Ophthalmol 1979; 63: 539-541
67 Amemiya T. Dark adaptation in diabetics. Ophthalmologica 1977; 174: 322-326
68 Ditzel J, Standl E. The oxygen transport system of red blood cells during diabetic ketoacidosis and recovery. Diabetologia 1975; 11: 255-260
69 Abu El-Asrar AM, Dralands L, Missotten L et al. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci 2004; 45: 2760-2766
70 Simó R, Hernández C. Neurodegeneration is an early event in diabetic retinopathy: Therapeutic implications. Br J Ophthalmol 2012; 96: 1285-1290