Graefes Arch Clin Exp Ophthalmol DOI 10.1007/s00417-014-2728-x

MISCELLANEOUS

The effect of cataract surgery on blue–yellow and standard-pattern visual-evoked potentials Matthias Fuest & Niklas Plange & Sarah Jamali & Hendrik Schwarzer & Gernot Roessler & Peter Walter & Babac Mazinani

Received: 31 January 2014 / Revised: 2 June 2014 / Accepted: 1 July 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Purpose Blue–yellow visual-evoked potentials (BY-VEPs) may be used for diagnostics of functional ganglion cell damage in glaucoma and other ocular diseases. In this study we investigated the impact of lenticular opacities on BY- and standard pattern reversal VEPs by examining patients before and after cataract surgery. Methods Eighteen patients with moderate cataract were included in a prospective study. Transient on/off isoluminant blue–yellow 2° checks were used for short-wavelength stimulation (BY-VEP), transient large 1° (M1) and small 0.25° (M2) black-white checks for standard pattern reversal VEPs. VEPs were acquired before (24 ± 30 days) and after cataract surgery (14 ± 16 days). The contralateral eye was used as a control. Results Amplitude and latency of M1 and M2 peaks did not change significantly from before to after surgery. The amplitude of the BY-VEPs did not change significantly after cataract surgery (pre-surgery, −7.42±3.43 μV, post-surgery, −7.93± 3.65 μV, p=0.42), yet the latency of the main negative peak showed a significant decrease (pre-surgery, 143.9±12.9 ms, post-surgery, 133.2±7.7 ms, p=0.0006). The BCVA improvement was significant from before to after cataract surgery (presurgery, 0.344±0.125 LogMAR, post-surgery, 0.224±0.179 LogMAR, p=0.013) yet not correlated to the absolute decrease in latency of the BY-VEP after surgery (r=0.309, p=0.22). No significant changes were found in the contralateral eye. Conclusions The BY-VEP is sensitive to lenticular opacities of the human lens, presumably due to the increased shortwavelength absorption in the aging eye. This fact should be considered when applying BY-VEPs for diagnostics. M. Fuest (*) : N. Plange : S. Jamali : H. Schwarzer : G. Roessler : P. Walter : B. Mazinani Department of Ophthalmology, RWTH Aachen University, Pauwelsstr. 30, 52074 Aachen, Germany e-mail: [email protected]

Keywords Visual-evoked potential . Chromatic . Short wavelength . Cataract surgery

Introduction Visual-evoked potentials (VEPs) are an essential tool in clinical and investigative ophthalmology as they allow an objective functional evaluation of the visual pathways from retina via the optic nerve to the visual cortex of the brain. In clinical practice, VEPs are used in the diagnosis of optic nerve diseases such as optic neuritis, optic atrophy, or compression of the optic pathways by tumors. Since the 1980s chromatic VEPs have received increasing attention for studying basic mechanisms of vision and clinical applications [1]. While achromatic large (parasol) ganglion cells project to the magnocellular layer of the lateral geniculate nucleus (LGN), the red–green pathway originates from smaller (midget) ganglion cells connected to parvocellular layers of the LGN. The blue–yellow pathway leads from bistratified ganglion cells to the interlaminar (koniocellular) neurons of the LGN [2]. Hence, chromatic VEPs allow the investigation of anatomically and physiologically distinct visual pathways. Crognale et al. applied chromatic visual-evoked potentials in numerous clinical settings and demonstrated specific alterations in for instance congenital and acquired color deficiencies [3], central serous choroidopathy [4] and optic neuritis, and multiple sclerosis [5]. Following the discovery that shortwavelength automated perimetry, using a blue stimulus on yellow background, can reveal visual field defects in patients with ocular hypertension before standard white-on-white perimetry [6], Horn et al. found alterations in shortwavelength VEPs of progressive glaucoma patients up to 2 years before optic nerve morphology changes were observed by fundus photographs [7].

Graefes Arch Clin Exp Ophthalmol

For standard-pattern VEPs, sources of error have been outlined, among them fixation losses, refractive errors, and visual acuity [8, 9]. For chromatic VEPs, research on this matter is scarce. Cataract has been described to affect standard-pattern VEP [10], yet its effect on BY-VEPs remains unclear. In this study, the effect of moderate cataract on BY-VEPs was investigated in patients undergoing standard cataract surgery. The influence of lenticular opacities on BY-VEPs as compared to standard-pattern VEPs was investigated and compared to the change in visual acuity.

Patients and methods Eighteen patients with moderate cataract planned for phacoemulsification were included in a prospective pilot study (14 men, four women; mean age, 69.2±8.8 years; range, 52.5-84.9 years). Patients with best-corrected visual acuity (BCVA) >0.50 LogMAR (±8dpt, alterations of the optical media other than cataract and cataracts graded nuclear color (NC), nuclear opalescence (NO), cortical (C), and posterior subcapsular (P)>3 LOCS III were excluded from the study. Out of our initial pool of 24 patients, we included 18 patients whose VEP peaks could be clearly measured in all tests. VEPs were conducted monocularly for both eyes before (mean time to surgery, 24±30 days) and after cataract surgery (mean time to surgery, 14±16 days). Adherence to the Declaration of Helsinki for research involving human subjects is confirmed. The study was approved by the institutional review board. The study subjects underwent phacoemulsification under regional (topical) or general anesthesia with intracapsular lens implantation. All operations were performed by one experienced surgeon (NP). Phakoemulsification was followed by intracapsular implantation of a foldable acrylic lens (CT Asphina 409MP, Carl Zeiss Meditec, Germany). VEPs were performed before and after surgery by an experienced technician (CK). The contralateral eye was used as a control.

checks were performed with a stimulation frequency of 1.5 Hz and a contrast of 97 % in coherence with ISCEV standard criteria [11]. Half-height view angle was 8.5°. Electrodes were placed according to the 10/20 system with the neutral electrode in the forehead position [12]. Participants’ refractive status was corrected for near vision depending on the testing distance (M1 and M2=1 meter; BY-VEPs=36 cm). One hundred trials were used to obtain averaged amplitude and peak time measurements. Latency and amplitude for M1 and M2 refer to the main positive peak (range M1, 89.1– 143.6 ms; range M2, 123.0–155.3 ms). Amplitude was measured from the zero line to peak. Chromatic VEPs to date are not described in the ISCEV standard. Hence, we used a setup that has proven reliable responses before [13, 14]. The blue stimulus was set at 460 nm. Red and green monitor phosphors were modified relying on a MacLeod-Boynton-Derrington-KrauskopfLennie (MBDKL) three-dimensional color space to generate an isoluminant yellow [4]. Wavelength was verified by the Colormeter C 2210 (LMT Lichtmesstechnik GmbH Berlin, Germany) and Eye One software (X-Rite GmbH Planegg, Germany. The CS-100A photometer (Minolta Corporation Tokyo, Japan) was used for gamma correction of our CRT monitor to ensure isoluminance. Testing began with a 2-min adaptation period to the yellow screen. Blue checks were then presented (200 ms on/911 ms off) on a yellow background with a frequency of 0.9 Hz. Chromatic contrast was 90 %, checkerboard size 2°, correlating to a spatial frequency of 0.25 c/deg with a half-height view angle of 20.6°. Latency and amplitude for BY-VEP refer to the main negative peak (range, 115.6–168.0 ms). Amplitude was measured from the zero line to peak.

Statistical analysis Correlations were tested using Fisher’s r to z test. Results of all 18 patients were averaged. For M1 and M2, amplitude and latency for the positive P100 peak and for BY-VEP for the main negative peak were analyzed and pre- and post-surgery results compared using a paired t test. P < 0.05 was considered significant.

Stimuli and recording

Results

The visual stimuli used for monocular VEP recording were presented on a color monitor (Maxdata, Marl, Germany). Pattern chromaticity, contrast, orientation, spatial frequency, and temporal profile were under computer control (Retisystem, Roland Consult, Brandenburg an der Havel, Germany). Transient pattern-reversal VEPs elicited by checkerboard stimuli with large 1° (M1) and small 0.25° (M2)

On the operated eye, amplitude and latency of M1 and M2 peaks of the standard achromatic VEPs did not change significantly from before to after surgery. The amplitude of the BY-VEPs did not change significantly after cataract surgery, yet the latency of the main negative peak showed a significant decrease. Figure 1 shows a representative change in the M1-VEP of a 62-year-old male patient

Graefes Arch Clin Exp Ophthalmol 5 4 3 2

Amplitude ( V)

Fig. 1 M1-VEPs of a 62-yearold male patient before and after cataract surgery. BCVA improved from 0.5 decimal to 1.0. Latency of the main positive peak decreased from 139.5 to 135.9 ms and amplitude increased from 3.1 to 4.9 μV after surgery

1 0 -1 -2 M1-VEP pre-surgery Datenreihe1 -3 M1-VEP post-surgery Datenreihe2 -4 -5 0

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(Fig. 2. M2). BCVA improved from 0.5 decimal to 1.0 after surgery. Latency of the main positive peak decreased from 139.5 to 135.9 ms and amplitude increased from 3.1 to 4.9 μV after surgery. Figure 3 shows the changes in the BY-VEPs of the same patient. Latency decreased from 168.0 to 140.6 ms and amplitude increased from −3.92 to −5.26 μV. All VEP data are presented in Table 1. On the non-surgical eye, no significant changes in amplitude or latency were found (data not shown). BCVA improved significantly from before to after cataract surgery (BCVA pre-surgery, LogMAR 0.344 ± 0.125/ BCVA post-surgery, LogMAR 0.224±0.179; p=0.013). The change in BCVA was not significantly correlated to

the decrease in latency of the BY-VEP after surgery (r=0.309, p=0.22, Fig. 4). The coefficient of variation was similar for M1 (M1 amplitude pre-surgery, 69.4 %; post-surgery, 52.2 %/ M1 latency pre-surgery, 13.6 %; post-surgery, 11.5 %), M2 (M2 amplitude pre-surgery, 42.3 %; post-surgery, 42.9 %/ M2 latency pre-surgery, 6.8 %; post-surgery, 6.5 %) and BY (BY amplitude pre-surgery, 46.9 %; postsurgery, 46.0 %/ BY latency pre-surgery, 8.9 %; postsurgery, 5.8 %). The coefficients of variation were higher for the amplitudes compared to the latencies. The coefficients of variation were similar for each parameter pre-surgery compared to post-surgery.

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Fig. 2 M2-VEPs of the patient from Fig. 1. Latency of the main positive peak decreased from 133.0 to 129.5 ms and amplitude increased from 4.6 to 6.1 μV after surgery

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Graefes Arch Clin Exp Ophthalmol Fig. 3 BY-VEPs of our patient from Fig. 1. Latency of the main negative peak decreased from 168.0 to 140.6 ms and amplitude increased from −3.92 to −5.26 μV after surgery

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Discussion In this study, no significant effect of cataract surgery on achromatic standard pattern VEPs with check sizes of 1° (M1) and 0.25° (M2) was found. Transient on/off BYVEPson the other hand showed a significant decrease in latency of the main negative peak. The amplitude was not significantly affected. The changes are not correlated to the changes in visual acuity. This implies that the BY latency decrease is presumably due to the increase of chromatic contrast following the abolishment of short-wavelength absorption by the cataractous lens and not primarily a function of BCVA improvement. The interindividual variability, as measured by the coefficient of variation, was much lower for latency than for amplitude in all our VEPs, which coincides with the current literature [15]. However pre- to post-surgery coefficients were similar and no difference between standard pattern and BYVEPs was found. Table 1 Comparison of latency (ms) and amplitude (μV) of main peak of standard achromatic VEPs (M1 and M2) and BY VEPs before (pre) and after (post) surgery. Mean and SD are presented

M1 amplitude M1 latency M2 amplitude M2 latency BY amplitude BY latency

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p value

6.6±4.23 120.2±16.4 6.14±2.60 140.7±9.6 −7.42±3.43 143.9±12.9

6.57±3.43 116.5±13.4 6.61±2.84 139.6±9.1 −7.93±3.65 133.2±7.7

0.41 μV −3.7 ms 0.47 μV −1.1 ms −0.51 μV −10.7 ms

0.42 0.063 0.42 0.65 0.42 0.0006

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Spekreijse already described in his thesis in 1966 that VEP examinations depend on the contour sharpness of the stimulus [16], hence the effect of cataract on standard pattern VEPs depends largely on the reduction of visual acuity. Lens opacities are believed to affect VEPs and other electrophysiological methods by defocusing and by light absorption [17]. Light scatter also seems to be of major importance, as it was recently shown for the multifocal electroretinogram (mfERG) [18]. For generating VEPs in cataractous eyes, contrast and check size are equally important. The better the visual acuity, the smaller the checks, and the lower the contrast can be to still produce acceptable responses [19]. Garcia-Martin et al. investigated achromatic transient standard pattern VEPs of 35 retinitis pigmentosa patients before and after cataract surgery. Similar to our results, no significant decrease of latency was witnessed. Yet the increase in amplitude of the P100 peak reached significance in this study [20]. This might be due to the larger number of patients and the greater improvement of BCVA (0.38 decimal; from 0.10±0.23 to 0.48±0.21). In our study, only patients with moderate cataract (LOCS III grading

The effect of cataract surgery on blue-yellow and standard-pattern visual-evoked potentials.

Blue-yellow visual-evoked potentials (BY-VEPs) may be used for diagnostics of functional ganglion cell damage in glaucoma and other ocular diseases. I...
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