Light-adapted electroretinograms of eyes with cataract recorded using the HE-2000 system before and after mydriasis

doi:10.21203/rs.3.rs-5315258/v1

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Light-adapted electroretinograms of eyes with cataract recorded using the HE-2000 system before and after mydriasis

https://doi.org/10.21203/rs.3.rs-5315258/v1

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Purpose

To evaluate the effectiveness of the non-mydriatic mode of the HE-2000 electroretinogram (ERG) by comparing photopic ERGs of non-mydriatic versus dilated eyes.

Methods

This retrospective observational study included patients with grade 2 cataracts between January and July 2022. Photopic ERGs were recorded using the HE-2000 system in mydriatic eyes, using a standard 3 cd·s/m² flashing stimulus, and non-mydriatic eyes, using the non-mydriatic mode with a 10 cd·s/m² stimulus. Amplitudes and implicit times of the a-wave, b-wave, and flicker ERG were compared between both conditions using the Wilcoxon signed-rank test. Correlations between these parameters were analyzed using Spearman’s rank correlation coefficient.

Results

In 54 eyes of 27 participants, the b-wave and flicker ERG amplitudes were significantly lower in non-dilated eyes than in dilated ones, with prolonged implicit times in the former (p < 0.0001). Despite these differences, b-wave and flicker ERG amplitudes and implicit times strongly correlated between dilated and non-dilated eyes (p < 0.01). However, the a-wave amplitude was more variable and less reliably measured in non-dilated eyes.

Conclusion

The HE-2000 system can produce clinically useful ERG recordings in non-dilated eyes, particularly for b-waves and flicker responses. Further validation under non-mydriatic conditions is necessary to establish its clinical utility.

Health sciences/Medical research

Health sciences/Biomarkers/Diagnostic markers

Electroretinography

photopic ERG

non-mydriatic

HE-2000 system

Cone ERG

Flicker ERG

Electroretinography (ERG) is widely used to objectively assess retinal function. Photopic ERGs include the light-adapted (LA) 3 ERG and LA 30 Hz flicker ERG. The LA 3 ERG induces responses in the cone system, manifested as a-waves arising from cone photoreceptors and OFF-bipolar cone cells and b-waves from both ON- and OFF-cone bipolar cells, whereas the LA 30 Hz flicker ERG records a sensitive cone-pathway-driven response. Photopic ERGs are helpful for monitoring cone function in degenerative retinal diseases, such as retinitis pigmentosa and cone dystrophy ^1–4; they are also used to evaluate retinal vascular ischemia, such as in diabetic retinopathy ^5,6 or central retinal vein occlusion ^7–10.

According to the standard protocols of the International Society of Clinical Electrophysiology of Vision (ISCEV), pupils should be fully dilated prior to ERG to avoid any influence from changes in pupil size and to maximize the field of retinal stimulation ¹¹. Tropicamide is a widely available choice for pupillary dilatation¹²; however, it has ocular adverse events, including transient stinging, photophobia, superficial punctate keratitis, blurred vision, increased intraocular pressure, and allergic reaction. Additionally, precipitating acute angle closure is a frequent concern for many clinicians in patients with certain anatomical features, such as shallow anterior chamber depth, short axial length, plateau iris configuration, or thick lenses ¹³. Thus, mydriasis-free ERGs would be safer, more practical, and more convenient for both clinicians and patients.

ERG electrodes are available in several forms, including contact lenses, conductive fibers and foils, conjunctival wire loops, corneal wicks, and skin electrodes ¹¹. Electrodes that are in contact with the cornea or bulbar conjunctiva are commonly used; however, these present several problems, such as corneal abrasion ¹⁴, difficulty with special populations such as children and the elderly, and potential concerns of infection, especially before and after surgery. In contrast, skin electrodes are less invasive, easy to use even for children ¹⁵ and the elderly, and safer during perioperative periods.

The RETeval system (LKC Technologies, Inc., Gaithersburg, MD, USA) has been available as an ERG that utilizes skin electrodes, and many studies have assessed its accuracy and the reproducibility of its results ^16–18. However, despite the aforementioned advantages of skin electrodes, they have been linked with problems associated with high noise levels and relatively lower amplitudes compared to conventional corneal electrodes ^17,19.

Another skin-electrode-based ERG system is the HE-2000 (Tomey Corporation, Nagoya, Japan) which has been available since February 2021 as a full-field ERG system ²⁰. Similar to the RETeval system, the HE-2000 system features a small handheld Ganzfeld dome and an original skin-electrode array and can record photopic ERGs from non-dilated eyes. However, the HE-2000 system differs from the RETeval system in three aspects. First, the HE-2000 system can simultaneously record cone and flicker ERGs in both eyes, reducing the recording time. Second, the HE-2000 is equipped with a newly developed subtraction system to reduce noise, a known problem with skin electrodes ²¹. Third, for non-dilated eyes, the HE-2000 system only delivers a stimulus with constant luminance (cd·s/m²) whereas the RETeval system delivers that with constant retinal illuminance (Td·s).

With the RETeval system, the stimulus intensity is dynamically adjusted based on the pupil size to maintain a constant retinal illuminance equal to the luminance multiplied by the pupil area ²². However, the HE-2000 system has no pupil monitoring function and only delivers constant luminance. Therefore, the HE-2000 system needs to be validated for recording in non-dilated pupils. In this study, we sought to evaluate the effectiveness of non-mydriatic ERG measurements performed using the HE-2000 system in patients with cataract by comparing the amplitudes and implicit times of photopic ERGs under non-mydriatic and mydriatic conditions.

Study population

The baseline characteristics of the participants are shown in Table 1. We studied 54 eyes of 27 patients with cataract (14 males and 13 females). The average age was 78.1 ± 7.5 years. The distribution of cataract types was identical between the right and left eyes, with 12 nuclear cataracts and 15 cortical cataracts in each. Axial length was 23.9 ± 1.1 mm in the right eyes and 23.7 ± 1.0 mm in the left eyes. The mean best corrected visual acuity (BCVA, measured as logarithms of the minimum angle of resolution [LogMAR]) was 0.27 ± 0.26 in the right eyes and 0.39 ± 0.42 in the left eyes.

Table 1

Baseline patient characteristics.
	N = 27
Male sex (%)	14, (51.9)
Age (years), mean ± SD	78.1 ± 7.5
Cataract type (%)
Right eyes
Nuclear	12, (44.4)
Cortical	15, (55.6)
Left eyes
Nuclear	12, (44.4)
Cortical	15, (55.6)
Axial length, mean ± SD
Right eyes	23.9 ± 1.1
Left eyes	23.7 ± 1.0
LogMAR BCVA, mean ± SD
Right eyes	0.27 ± 0.26
Left eyes	0.39 ± 0.42
SD, standard deviation; logMAR, logarithm angle of resolution; BCVA, best corrected visual acuity.

Comparing mydriatic and non-mydriatic ERG measurements

Cone ERG and flicker ERG parameters were compared using the Wilcoxon signed-rank test. Data for the right and left eyes are presented in Table 2.

Table 2

Comparison of Cone and Flicker ERG parameters between non-mydriatic and mydriatic eyes.
			Right eyes (N = 27)			Left eyes (N = 27)
			Non-mydriatic	Mydriatic	P-value	Non-mydriatic	Mydriatic	P-value
Cone ERG	a-wave	Amplitude	9.54 ± 3.50	11.83 ± 4.72	0.12	10.22 ± 3.82	10.81 ± 2.49	0.400
		Implicit time	17.17 ± 1.64	16.17 ± 3.10	< 0.01	17.22 ± 1.65	15.56 ± 1.55	< 0.0001
	b-wave	Amplitude	33.19 ± 10.92	40.13 ± 10.93	< 0.0001	32.47 ± 13.17	39.60 ± 11.47	< 0.0001
		Implicit time	34.33 ± 1.56	30.85 ± 1.44	< 0.0001	34.02 ± 4.06	30.96 ± 1.38	< 0.0001
Flicker ERG		Amplitude	17.79 ± 5.97	25.47 ± 8.39	< 0.0001	18.09 ± 6.95	25.38 ± 9.41	< 0.0001
		Implicit time	29.54 ± 3.09	28.17 ± 2.20	< 0.01	29.76 ± 3.08	27.81 ± 2.77	< 0.0001
ERG, electroretinography; SD, standard deviation. The parameters were compared between non-mydriatic and mydriatic eyes using the Wilcoxon signed-rank test.

Regarding the right eyes, the a-wave amplitude was 9.54 ± 3.50 µV in non-mydriatic eyes and 11.83 ± 4.72 µV in mydriatic eyes (p = 0.12), with an implicit time of 17.17 ± 1.64 msec and 16.17 ± 3.10 msec in each, respectively (p < 0.01); the b-wave amplitude was 33.19 ± 10.92 µV in non-mydriatic eyes and 40.13 ± 10.93 µV in mydriatic eyes (p < 0.0001), with an implicit time of 34.33 ± 1.56 msec and 30.85 ± 1.44 msec in each, respectively (p < 0.0001); and the flicker ERG amplitude was 17.79 ± 5.97 µV in non-mydriatic eyes and 25.47 ± 8.39 µV in mydriatic eyes (p < 0.0001), with an implicit time of 29.54 ± 3.09 msec and 28.17 ± 2.20 msec in each, respectively (p < 0.01).

Regarding the left eyes, the a-wave amplitude was 10.22 ± 3.82 µV in non-mydriatic eyes and 10.81 ± 2.49 µV in mydriatic eyes (p = 0.40), with an implicit time of 17.22 ± 1.65 msec and 15.56 ± 1.55 msec in each, respectively (p < 0.0001); the b-wave amplitude was 32.47 ± 13.17 µV in non-mydriatic eyes and 39.60 ± 11.47 µV in mydriatic eyes (p < 0.0001), with an implicit time of 34.02 ± 4.06 msec in and 30.96 ± 1.38 msec in each, respectively (p < 0.0001); and the flicker ERG amplitude was 18.09 ± 6.95 µV in non-mydriatic eyes and 25.38 ± 9.41 µV in mydriatic eyes (p < 0.0001), with an implicit time of 29.76 ± 3.08 msec and 27.81 ± 2.77 msec in each, respectively (p < 0.0001).

Furthermore, we investigated the correlations between these parameters in non-mydriatic and mydriatic eyes using Spearman’s rank correlation coefficient. Data for the right and left eyes are presented in Table 3. Regarding the right eyes, the correlation coefficients for the amplitude and implicit time of the a-wave were − 0.01 (p = 0.92) and 0.18 (p = 0.36), respectively; the correlation coefficients for the amplitude and implicit time of the b-wave were 0.70 (p < 0.0001) and 0.45 (p < 0.05), respectively; and the correlation coefficients for the amplitude and implicit time of the flicker ERG were 0.90 (p < 0.0001) and 0.51 (p < 0.01), respectively. Regarding the left eyes, the correlation coefficients for the amplitude and implicit time of the a-wave were 0.47 (p < 0.05) and 0.28 (p = 0.15), respectively; the correlation coefficients for the amplitude and implicit time of the b-wave were 0.56 (p < 0.01) and 0.59 (p < 0.01), respectively; and the correlation coefficients for the amplitude and implicit time of the flicker ERG were 0.85 (p < 0.0001) and 0.78 (p < 0.0001), respectively.

Table 3

The correlation coefficient of Cone ERG and Flicker ERG parameters between non-mydriatic eyes and mydriatic eyes.
			Right eyes (N = 27)		Left eyes (N = 27)
			R	P-value	R	P-value
Cone ERG	a-wave	Amplitude	-0.01	0.92	0.47	< 0.05
		Implicit time	0.18	0.36	0.28	0.15
	b-wave	Amplitude	0.70	< 0.0001	0.56	< 0.01
		Implicit time	0.45	< 0.05	0.59	< 0.01
Flicker ERG		Amplitude	0.90	< 0.0001	0.85	< 0.0001
		Implicit time	0.51	< 0.01	0.78	< 0.0001
ERG, electroretinography. The correlations were assessed using Spearman’s rank correlation coefficient.

This study is the first to report on the newly developed skin-electrode-based HE-2000 system. Our findings demonstrate that b-wave and flicker amplitudes were significantly lower, and implicit times of the a-and b-waves of the cone and flicker responses were longer, in non-dilated eyes compared to dilated eyes. However, the amplitudes of the b-waves of the cone response and flicker ERGs showed strong correlations between non-dilated and dilated eyes.

Skin electrodes tend to produce more noise than other electrode types, potentially hindering the accurate measurement of a-waves. This could be due to electrical interference, which reduces the sensitivity of the recordings, particularly for low-amplitude responses like the a-wave. This limitation should be considered when interpreting results from the HE-2000 system.

A previous study investigated the effect of a non-dilated pupil on the photopic and scotopic luminance response function ²³; they confirmed prolonged a- and b-wave implicit times in non-dilated eyes than in dilated ones. These longer implicit times were normalized after increasing the background luminance from 25 cd/m² to 80 cd/m². Therefore, it might be feasible for the HE-2000 system to record implicit times in non-dilated pupils closer to those in dilated pupils by increasing background illumination. However, the current HE-2000 system does not allow adjustments to the default background illumination of 30 cd/m², precluding further assessment. Future iterations of the system should incorporate an adjustable interface for background illumination.

Normalizing the amplitude in non-dilated eyes presents a greater challenge than normalizing implicit time. A previous report indicated a rightward shift of the photopic luminance-response function, with the highest amplitude achieved at 3.9 cd·s/m² in dilated eyes but 10.6 cd·s/m² in non-dilated ones ²³. This nearly three-fold increase in luminance required for maximum response in non-dilated eyes may justify the HE-2000’s default setting of 10 cd·s/m² for non-mydriatic mode as opposed to the 3 cd·s/m² used in mydriatic mode. However, the same study reported that even with sufficient luminance, non-dilated eyes yielded maximum amplitudes up to only 14% lower than dilated ones ²³. This difference may be attributed to the smaller pupillary apertures in non-dilated eyes, which limit the amount of light reaching peripheral cone photoreceptors compared to dilated pupils. Notably, the study reported that the maximum response could not be normalized, even with changing the background luminance ²³. This suggests that non-dilated eyes require a different reference range of amplitudes than dilated ones.

A previous study that employed the RETeval system in eyes with cataract reported no significant difference in the flicker ERG amplitudes and implicit times between dilated and non-dilated eyes ²⁴. In contrast, our study employing the HE-2000 system observed lower flicker ERG amplitudes and longer implicit times in non-dilated eyes compared to dilated ones. This discrepancy maybe attributed to be the inability of the HE-2000 system to deliver constant retinal illuminance. The RETeval system can deliver constant retinal illuminance (Td·s), whereas the HE-2000 system can only deliver constant luminance (cd·s/m²); this difference may influence the flicker ERG results, as a flash stimulus of 10 cd·s/m² in non-dilated eyes may be insufficient to produce retinal illuminance equivalent to that in dilated eyes.

A previous study investigated the differences between constant luminance and constant retinal illuminance in flicker ERGs ²⁵, demonstrating that constant retinal illuminance results in less intra-subject variability ²⁵. This suggests that the RETeval system, by delivering constant retinal luminance, reduces variations in retinal stimulation caused by pupillary changes and provides narrower reference ranges compared to the HE-2000 system. Thus, compared to the RETeval, the HE-2000 system has the disadvantage of being unable to deliver constant retinal illuminance; however, the HE-2000 offers the advantage of simultaneous binocular measurements.

Sugawara et al. highlighted the inability of the RETeval system to perform simultaneous binocular measurements as a disadvantage ²⁶. In their study, they measured flicker ERGs twice in the same subject across two sessions using RETeval; the first measurement was taken in the right eye followed by the left eye, and the second measurement was taken in the left eye followed by the right eye. They observed a prolongation of implicit times in the second session compared to the first, indicating potential measurement inconsistencies unless protocols were established in advance. The HE-2000 system, with its simultaneous binocular measurement capability, eliminates this potential variability. However, achieving simultaneous real-time pupil monitoring in both eyes presents technical challenges ²⁶. Ultimately, the RETeval system's constant retinal illumination and the HE-2000 system's simultaneous binocular measurement capability are considered a trade-off, making it difficult to definitively assess their overall superiority or inferiority. Further studies directly comparing the clinical usefulness of these two systems are necessary.

Another factor that warrants consideration is the use of skin electrodes. While less invasive and easier to apply than corneal electrodes, skin electrodes inherently introduce higher levels of noise. This may have contributed to the relatively low amplitude of the a-wave in non-mydriatic eyes, as the a-wave, representing a smaller, earlier response, may be more susceptible to noise interference, hindering their detection. Although the HE-2000 incorporates a subtraction system to reduce noise, it may not have been sufficient to mitigate this issue entirely, particularly in non-mydriatic recordings, where the signal-to-noise ratio may already be compromised.

Despite these limitations, our study demonstrated a strong correlation between the amplitude and implicit time of the b-wave and flicker ERG responses in both dilated and non-dilated eyes. This suggests that clinically relevant measurements can be obtained even from non-mydriatic eyes provided that appropriate correction factors or formulas are applied. Such corrections could enable safer and more practical ERG recordings, especially in situations where pupil dilation is not feasible or advisable.

In addition to the aforementioned considerations, this study had several limitations. First, pupil diameter was not measured during the ERG recordings, precluding a comprehensive assessment of the impact of pupillary constriction on photopic ERG responses. Future studies should incorporate pupil monitoring to better understand the influence of the natural pupil size on the recorded signals. Second, the HE-2000 system’s continuous measurement mode, employed in this study, deviates from ISCEV standards. Consequently, the findings may not be directly comparable to those of other ERG studies adhering to standard protocols. Validation of this continuous mode is necessary to establish its clinical relevance. Third, we focused exclusively on photopic ERG recordings and did not evaluate scotopic ERG responses. Further research is required to assess the system's performance under scotopic conditions, particularly in non-dilated eyes. Finally, the relatively small sample size limits the generalizability of the results. Further studies with larger cohorts are needed to validate these findings.

In conclusion, this study demonstrated that the HE-2000 system can effectively measure photopic ERG responses in both dilated and non-dilated eyes, although amplitudes and implicit times differ between the two conditions. Despite these differences, the strong correlation between b-wave and flicker ERG responses in dilated and non-dilated eyes suggests that clinically useful data can still be obtained without pupillary dilation, particularly with the application of appropriate correction formulas. Further studies are necessary to optimize the system’s performance under non-mydriatic conditions and further explore its potential utility across diverse patient populations.

This was a retrospective observational study that included patients with cataract between January and July 2022. Each patient had received a comprehensive ophthalmic examination, including measurements of BCVA and intraocular pressure, slit-lamp examination, and indirect ophthalmoscopy. A monocular Landolt ring chart (System Charts SC-2000; Nidek Instruments, Gamagori, Japan) was used to measure BCVA at 5 m. For the statistical analysis, the decimal values of BCVA were converted to logMAR ones. Cataracts were graded based on the Emery-Little classification system ²⁷, and only patients with bilateral grade 2 cataracts were included. Patients with any corneal, retinal, or choroidal disease or refractive error (myopia > -6.00 diopters or hyperopia > + 3.00 diopters) were excluded.

This study involved a retrospective review of hospital medical records and adhered to the tenets of the Declaration of Helsinki. The study protocol was approved by the Ethics Committee of Suwa Red Cross Hospital (approval no. 4 − 3). Patients were notified of the study through the hospital's website and were provided with the option to decline participation.

The HE-2000 system used in this study consisted of a handheld device (HE-2000; 130 × 171 × 130 mm; weight, 260 g) for stimulating, recording, and analyzing the signals; a docking station (HE-2010; 140 × 168 × 165; weight, 1.6 kg) for charging and exporting the results to a computer; and disposable skin electrodes for picking up the electrical signals (Fig. 1a, b). It was capable of recording all ISCEV-ERG standard tests, including Rod ERG (dark-adapted 0.01 ERG), Flash ERG・SF3 (dark-adapted 3 ERG), Flash ERG・BF10 (dark-adapted 10 ERG), oscillatory potentials, Cone ERG (LA 3 ERG), and Flicker ERG (LA 30 Hz flicker ERG). Two available continuous recording modes were used: the scotopic mode for recording Rod and flash ERGs and photopic mode for recording Cone and flicker ERGs. These two modes can shorten the examination time and output the results in a single datasheet. The handheld device (HE-2000) was portable and had a rechargeable lithium battery and a wireless connection to the docking station to send the recorded data. A small-diameter dome produced a full-field stimulus. A small red fixation spot was displayed at the center of the Ganzfeld dome, and the patients were instructed to fix their gaze on this spot during the examination.

The manufacturer recommends recording in mydriatic mode, under full bilateral pupil dilatation, although a non-mydriatic mode is also available. In the non-mydriatic mode, the stimulus flash luminance (cd·s/m²) increases six-fold in Rod ERG and three-fold in the other ERGs.

For performing the ERGs, a skin electrode array was attached to the patient’s orbital rim, 5 mm from the inferior eyelid margin. The electrodes could be active (positive), reference (negative), or ground. The recorded electrical potentials were DC-amplified and digitized.

The HE-2000 was operated according to the written instructions provided by the manufacturer. Recordings were performed using the recommended default settings of 3 cd·s/m² stimulus flash luminance for the Cone and Flicker ERGs in mydriatic mode and 10 cd·s/m² in non-mydriatic mode; background illumination was 30 cd·s/m².

For mydriatic ERG measurements, pupillary dilation was induced using topical tropicamide and phenylephrine. A pupil diameter of 6 mm or more was confirmed before the ERG exam. Before recording, the patients were light-adapted for 10 min under room light. The ground electrode was placed at the midpoint between the left eye and ear. The reference electrode was placed on the lower eyelid.

Voltage changes were simultaneously recorded in both eyes during stimulation. For noise reduction, voltage changes in the non-stimulated eye were subtracted from those in the stimulated eye, and to further reduce noise, we averaged the responses of 16 flashes for LA3 ERG and 32 flashes for flicker ERG for each eye. The representative case is shown in Fig. 2.

Statistical analysis

Statistical analyses were performed using GraphPad Prism (version 10.2.3; GraphPad Software, San Diego, CA, USA). Continuous data are presented as means ± standard deviation, and categorical data are expressed as counts and percentages. The data were analyzed using the Wilcoxon signed-rank test to compare parameters between non-mydriatic and mydriatic eyes. Correlations between the amplitudes and implicit times under non-mydriatic and mydriatic conditions were assessed using Spearman’s rank correlation coefficient. For all statistical tests, a p-value of less than 0.05 was considered statistically significant.

Acknowledgments

We would like to thank Editage (www.editage.com) for the English language editing.

Author contributions

Study design, TH, YC, and TM; data gathering, YC, SI, and KA; data interpretation, TH and YC; and manuscript drafting, TH, YC, and TM.

Data availability statement

The datasets generated and/or analyzed during the current study are not publicly available due to institutional policy on patient data confidentiality but are available from the corresponding author upon reasonable request.

Ethics declarations

This study involved a retrospective review of hospital medical records and adhered to the tenets of the Declaration of Helsinki. The study protocol was approved by the Ethics Committee of Suwa Red Cross Hospital (approval no. 4-3). Informed consent was waived for this study by the Ethics Committee of Suwa Red Cross Hospital, as the research involved retrospective data analysis of de-identified patient information without any intervention affecting patient care. Instead, in accordance with the instructions of the ethics committee, an option to opt out is presented on the hospital’s website.

Additional information

Conflicts of Interest: Takao Hirano received personal fees from Novartis Pharma K.K., Bayer, Canon, Kowa Pharmaceutical, Senju Pharmaceutical, Chugai Pharmaceutical, and Santen Pharmaceutical. Toshinori Murata received personal fees from Novartis Pharma K.K., Bayer, Canon, Kowa Pharmaceutical, Senju Pharmaceutical, Chugai Pharmaceutical, Kyowa Kirin, and Santen Pharmaceutical. The other authors have no conflicts of interest to disclose. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Competing interest reported. Conflicts of Interest: Takao Hirano received personal fees from Novartis Pharma K.K., Bayer, Canon, Kowa Pharmaceutical, Senju Pharmaceutical, Chugai Pharmaceutical, and Santen Phar-maceutical. Toshinori Murata received personal fees from Novartis Pharma K.K., Bayer, Canon, Kowa Pharmaceutical, Senju Pharmaceutical, Chugai Pharmaceutical, Kyowa Kirin, and Santen Pharmaceutical. Other authors have no conflicts of interest to disclose.

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Light-adapted electroretinograms of eyes with cataract recorded using the HE-2000 system before and after mydriasis

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Abstract

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Introduction

Results

Study population

Comparing mydriatic and non-mydriatic ERG measurements

Discussion

Materials and methods

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Version 1