The Role of Electroretinography in Assessing the Progression of Diabetic Retinopathy

Su Eun Park; Hae Jung Sun; Hyun Joon Lee; Tae Kwann Park; Young-Hoon Ohn

doi:10.3341/jkos.2010.51.5.693

Journal List > J Korean Ophthalmol Soc > v.51(5) > 1008810

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Park, Sun, Lee, Park, and Ohn: The Role of Electroretinography in Assessing the Progression of Diabetic Retinopathy

Original Article

J Korean Ophthalmol Soc 2010;51(5):693-699.

Published online: 25 September 2010

DOI: https://doi.org/10.3341/jkos.2010.51.5.693

The Role of Electroretinography in Assessing the Progression of Diabetic Retinopathy

Su Eun Park, MD¹, Hae Jung Sun, MD², Hyun Joon Lee, MD², Tae Kwann Park, MD², Young-Hoon Ohn, MD^2,

¹Department of Ophthalmology, Hallym University College of Medicine, Seoul, Korea

²Department of Ophthalmology, Soonchunhyang University College of Medicine, Bucheon, Korea

Address reprint requests to Young-Hoon Ohn, MD Department of Ophthalmology, Soonchunhyang University, College of Medicine #1174 Jung-dong, Wonmi-gu, Bucheon 420-767, Korea Tel: 82-32-621-5053, Fax: 82-32-621-5435, E-mail: yhohn@schbc.ac.kr

Received 22 April 2009 Accepted 23 February 2010

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Purpose

To investigate the clinical significance of electroretinographic (ERG) responses, including the photopic negative response parameter, in assessing the progression of diabetic retinopathy.

Methods

Standard flash ERG was tested on 28 normal controls and 143 patients who were diagnosed with diabetes mellitus. Of those, 97 patients had diabetic retinopathy in different stages. Electroretinography was performed according to the International Society for Clinical Electrophysiology of Vision (ISCEV) standards. Amplitudes and implicit times of ERG responses, including the photopic negative response (PhNR), were compared at different stages of diabetic retinopathy.

Results

Amplitudes of oscillatory potentials were significantly reduced in mild NPDR. Cone b-wave amplitude, 30-Hz flicker response, and PhNR were significantly reduced in moderate NPDR.

Conclusions

These results suggest that oscillatory potentials are good indicators of retinal function change in the early stage of diabetic retinopathy, and the appropriate results of the cone b-wave, 30-Hz flicker response and PhNR tests are good indicators of moderate NPDR.

Keywords: Diabetic retinopathy, Oscillatory potentials, Photopic negative response, Standard electroretinography

References

1. Wallow IH, Engerman RL. Permeability and patency of retinal blood vessels in experimental diabetes. Invest Ophthalmol Vis Sci. 1977; 16:447–61.

2. Wallow IH, Geldner PS. Endothelial fenestrae in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 1980; 19:1176–83.

3. Han YK, Ohn YH. Changes of ERG parameters in diabetic retinopathy. J Korean Ophthalmol Soc. 2000; 41:149–55.

4. Yonemura D, Kawasaki K. New approaches to ophthalmic electro-diagnosis by retinal oscillatory potentials, drug-induced responses from retinal pigment epithelium and cone potential. Doc Ophthalmol. 1974; 48:163–222.

5. Bresnick GH, Palta M. Temporal aspects of the electroretinogram in diabetic retinopathy. Arch Ophthalmol. 1987; 105:660–4.

6. Li Q, Zemel E, Miller B, Perlman I. Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp Eye Res. 2002; 74:615–25.

7. Bresnick GH, Palta M. Oscillatory potential amplitudes: Relation to severity of diabetic retinopathy. Arch Ophthamol. 1987; 105:929–33.

8. Ogden TE. Oscillatory waves of the primate electroretinogram. Vision Res. 1973; 13:1059–74.

9. Vigh J, Solessio E, Morgans CW, Lasater EM. Ionic mechanisms medi-ating oscillatory membrane potentials in wide-field retinal amacrine cells. J Neurophysiol. 2003; 90:431–43.

10. Hancock HA, Kraft TW. Oscillatory potential analysis and ERGs of normal and diabetic rats. Invest Ophthalmol Vis Sci. 2004; 45:1002–8.

11. Juen S, Kieselbach GF. Electrophysiological changes in juvenile abdominals without retinopathy. Arch Ophthalmol. 1990; 108:372–5.

12. Vadalà M, Anastasi M, Lodato G, Cillino S. Electroretinographic abdominal potentials in insulin-dependent diabetes patients:a long-term follow-up. Acta Ophthalmol Scand. 2002; 80:305–9.

13. Yoshida A, Kojima M, Ogasawara H, Ishiko S. Oscillatory potentials and permeability of the blood-retinal barrier in noninsulin-dependent diabetic patients without retinopathy. Ophthalmology. 1991; 98:1266–71.

14. Holopigian K, Seiple W, Lorenzo M, Carr R. A comparison of abdominal and scotopic electroretinographic changes in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 1992; 33:2773–80.

15. Seo DS, Lee SY, Park SK, Roh JH. Usefulness of standard abdominal in the early diagnosis of diabetic retinopathy: analysis abdominal Receiver Operating Characteristic (ROC) curve. J Korean Ophthalmol Soc. 1999; 40:1552–8.

16. Kwak MS, Kim SH. The electroretinogram a- and b-wave in diabetic retinopathy. J Korean Ophthalmol Soc. 1994; 35:1081–7.

17. Viswanathan S, Frishman LJ, Robson JG, et al. The photopic negative response of the macaque electroretinogram: reduction by abdominal glaucoma. Invest Ophthalmol Vis Sci. 1999; 40:1124–36.

18. Viswanathan S, Frishman LJ, Robson JG, Walters JW. The photopic negative response of the flash electroretinogram in primary open abdominal glaucoma. Invest Ophthalmol Vis Sci. 2001; 42:514–22.

19. Gotoh Y, Machida S, Tazawa Y. Selective loss of the photopic negative response in patients with optic nerve atrophy. Arch Ophthalmol. 2004; 122:341–6.

20. Colotto A, Falsini B, Salgarello T, et al. Photopic negative response of the human ERG: losses associated with glaucomatous damage. Invest Ophthalmol Vis Sci. 2000; 41:2205–11.

21. Ng YK, Zeng XX, Ling EA. Expression of glutamate receptors and calcium-binding proteins in the retina of streptozotocin-induced abdominal rats. Brain Res. 2004; 1018:66–72.

22. Pulido JE, Pulido JS, Erie JC, et al. A role for excitatory amino acids in diabetic eye disease. Exp Diabetes Res. 2007; 2007:36150.

23. Santiago AR, Hughes JM, Kamphuis W, et al. Diabetes changes abdominal glutamate receptor subunit expression level in the human retina. Brain Res. 2008; 1198:153–9.

24. Kizawa J, Machida S, Kobayashi T, et al. Changes of oscillatory abdominal and photopic negative response in patients with early diabetic retinopathy. Jpn J Ophthalmol. 2006; 50:367–73.

25. Kim HD, Park SH, Park SE, Ohn YH. Photopic negative response (PhNR) in normal subjects. J Korean Ophthalmol Soc. 2009; 50:1531–8.

26. Sieving PA, Frishman LJ, Steinberg RH. Scotopic threshold response of proximal retina in cat. J Neurophysiol. 1986; 56:1049–61.

27. Aylward GW. The scotopic threshold response in diabetic retinopathy. Eye. 1989; 3:626–37.

28. Attawia MA, Nayak RC. Circulating antipericyte autoantibodies in diabetic retinopathy. Retina. 1999; 19:390–400.

29. Kastelan S, Zjacić-Rotkvić V, Kastelan Z. Could diabetic retinopathy be an autoimmune disease? Medical Hypotheses. 2007; 68:1016–8.

Figure 1.

Amplitudes of ERG parameters of control and diabetic patients.

Figure 2.

Implicit times of ERG parameters of control and diabetic patients.

Figure 3.

The ROC curves of the amplitude of the eletroretinogram parameters.

Figure 4.

The ROC curves of the implicit time of the eletroretinogram parameters.

Table 1.

Age and sex distributions of normal control and diabetic groups

Group	Male	Female	Mean age (years)± SD^§ (Range)
Normal control group	17 (61%)	11 (39%)	44.4±8.8 (33∼63)
Diabetic case group	74 (51%)	69 (48%)	53.1±9.2 (30∼75)
0 (No retinopathy)	23	8	57.6 (43∼65)
1 (Mild NPDR)	8	15	52.9 (30∼68)
2 (Moderate NPDR)	14	25	54.5 (38∼75)
3 (Severe NPDR)	21	12	51.5 (43∼73)
4 (PDR)	8	9	46.1 (32∼59)
p-value	0.3	15^*	<0.001^#

^* p-value calculated by chi-square test

^# p-value calculated by student's t-test

^§ SD=standard deviation.

Table 2.

The changes in the amplitudes of ERG parameters in progression of diabetic retinopathy

Variables (Amplitude)	Normal		Group 0		Group 1		Group 2		Group 3		Group 4
Variables (Amplitude)	Mean	SD^#	Mean	SD	Mean	SD	Mean	SD	Mean	SD	Mean	SD
Maximal combined response
b-wave	444.0	66.9	373.6	65.8	375.2	85.4	291.4	72.3	296.9	136.6	231.7	72.2
Ops	257.0	58.6	175.0	51.6	137.4^*	32.9	110.7^*	50.3	99.2^*	45.0	69.7^*	19.1
Cone response
b-wave	170.1	46.9	132.9	28.3	134.7	35.0	97.8^*	28.4	98.1	38.0	73.4^*	25.4
PhNR	49.4	13.9	34.7	11.2	35.1	14.8	23.5^*	11.8	17.7^*	11.8	14.8^*	15.6
30Hz flicker response	119.3	24.9	94.2	20.7	90.0	25.5	66.6^*	17.8	66.8	23.6	54.4^*	19.0

^* Grouping by post-hoc test of ANOVA was significant (If p-value of ANOVA test is less than 0.05, then post-hoc test is done.)

^# SD=standard deviation.

Table 3.

The changes in the implicit times of ERG parameters in progression of diabetic retinopathy

Variables (Amplitude)	Normal		Group 0		Group 1		Group 2		Group 3		Group 4
Variables (Amplitude)	Mean	SD	Mean	SD	Mean	SD	Mean	SD	Mean	SD	Mean	SD
Maximal combined response	43.3	2.1	47.7	3.9	45.5	5.4	48.4^*	5.1	49.3^*	4.9	57.3^*	9.6
Cone response	30.7	1.4	31.3	2.9	30.8	1.2	32.5^*	6.3	33.3^*	3.8	38.6^*	4.8
PhNR	42.5	2.3	45.4	2.5	44.0	2.0	46.3	8.7	48.4	3.8	55.9	4.9
30Hz flicker response	27.5	1.3	29.0	1.3	28.5	2.0	32.0^*	3.3	32.7	3.3	34.4	5.5
Ops 1	18.2	1.7	18.5	2.0	18.6	1.8	19.5	4.3	19.9	4.4	19.4	6.9
Ops 2	24.8	2.1	25.1	2.1	25.4	1.8	27.4	5.0	27.9	6.7	31.3	10.9
Ops 3	32.6	2.7	33.5	3.7	33.8	3.2	36.3^*	5.3	37.9	6.4	38.3	8.6
Ops 4	42.3	2.8	43.6	3.7	45.0	5.0	45.8	4.7	48.0	6.3	48.0	6.1

SD=standard deviation

^* Grouping by post‐hoc test of ANOVA was significant (If p‐value of ANOVA test < 0.05, then post-hoc test was done).

Table 4.

AUC of the amplitude ROC curves

Variables (Amplitude)	AUC (Area under the curve)
Maximal combined response
b-wave	0.83
Ops	0.95
Cone response
b-wave	0.83
30Hz flicker res.	0.87
PhNR	0.89

Table 5.

AUC of the implicit time ROC curves

Variables (Implicit time)	AUC (Area under the curve)
Maximal combined response	0.85
Cone response	0.71
30Hz flicker response	0.83
PhNR	0.83
Oscillatory potential 1	0.61
Oscillatory potential 2	0.67
Oscillatory potential 3	0.73
Oscillatory potential 4	0.72

TOOLS

Similar articles