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Ultraviolet and Green Light Cause Different Types of Damage in Rat Retina

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Ultraviolet and Green Light Cause Different Types of Damage in Rat Retina Ultraviolet and Green Light Cause Different Types of Damage in Rat Retina Theo G. M. F. Gorgels? and Dirk van Norren*^ Purpose. To assess the influence of wavelength on retinal light damage in rat with funduscopy and histology and to determine a detailed action spectrum. Methods. Adult Long Evans rats were anesthetized, and small patches of retina were exposed to narrow-band irradiations in the range of 320 to 600 nm using a Xenon arc and Maxwellian view conditions. After 3 days, the retina was examined with funduscopy and prepared for light microscopy. Results. The dose that produced a change just visible in fundo was determined for each wavelength. This threshold dose for funduscopic damage increased monotonically from 0.35 J/cm2 at 320 nm to 1600 J/cm2 at 550 nm. At 600 nm, exposure of more than 3000J/cnr did not cause funduscopic damage. Morphologic changes in retinas exposed to threshold doses at wavelengths from 320 to 440 nm were similar and consisted of pyknosis of photorecep- tors. Retinas exposed to threshold doses of 470 to 550 nm had different morphologic appear- ances. Retinal pigment epithelial cells were swollen, and their melanin had lost the characteris- tic apical distribution. Some pyknosis was found in photoreceptors. Conclusions. Damage sensitivity in rat increases enormously from visible to ultraviolet wave- lengths. Compelling evidence is presented that two morphologically distinct types of damage occur in the rat retina, depending on the wavelength. Because two types also have been described in monkey, a remarkable similarity seems to exist across species. Invest Ophthahnol VisSci. 1995; 36:851-863. In 1966, Noell and coworkers1 reported that the rat ity and histologic site of damage. Studies on mon- retina can be damaged by light even when levels are keys2'3 and, recently, also on rats4S showed an increase well below the threshold for thermal damage. They in damage sensitivity for shorter wavelengths (with a postulated that the damage mechanism involves nox- maximum in the ultraviolet wavelengths). Damage was ious chemical reactions initiated by photon absorption sometimes found to manifest itself in photoreceptors, in a chromophore in the retina. whereas in other studies it was localized in RPE, Miiller In these first experiments on photochemical dam- cells, or mitochondria throughout the retinal lay- 1 3 6 9 age to the retina, damage was found in photoreceptors ers. - - " and the retinal pigment epithelium (RPE). The action These diverse observations suggest that multiple spectrum of damage resembled the rhodopsin absorp- types of retinal light damage exist, as review articles tion curve, which suggested that rhodopsin is the dam- have indicated.6'7''0>11 However, the characteristics and aging chromophore. Since then, many studies have classification of these types are not well established, been conducted on retinal light damage. Their out- mainly because the various studies differed substan- comes revealed a large variety in both spectral sensitiv- tially in experimental procedures, which makes it dif- ficult to deduce the critical factors that determine damage type. Wavelength is most likely one of these From the *F. C. Danders Institute of Ophthalmology, Ulreckt Academic Hospital, Utrecht, and the f National Aerospace Medical Center, Soeslerberg, The Netherlands. factors because photochemical reactions depend on Supported by a grant from the Dr. F. P. Fischer Foundation. absorption spectra of their chromophores.1'2 In the Submitted for publication April 12, 1994; revisedjune 27, 1994; accepted November 15, 1994. present study, we aimed at carefully exploring the fac- Proprietary interest category: N. tor wavelength in setting the threshold for retinal light Reprint requests: Theo G. M. F. Gorgels, F. C. Danders Institute of Ophthalmology, Utrecht Academic Hospital, P.O. Box 85500, 3508 GA, Utrecht, The Netherlands. damage. A detailed action spectrum was determined Investigative Ophtha nology & Visual Science, April 1995, Vol. 36, No. 5 Copyright © Associa on for Research in Vision and Ophthalmology 851 Downloaded from iovs.arvojournals.org on 10/02/2021 852 Investigative Ophthalmology & Visual Science, April 1995, Vol. 36, No. 5 P1 R' monochromator ss \ exit slit BBal^tk1* '• rat eye obsei transmission (%) FIGURE l. Irradiation optics. A set of neutral-density filters separated by black bands was placed at a plane conjugate to the retina (R'). Thus, four patches of retina were simultane- ously irradiated at different levels. P' is a plane conjugate to the pupil. P = pupil plane; R = retinal plane. with narrow-band irradiations. Because rat ocular me- rat eye. Two partly overlapping neutral-density filters dia transmit a large portion of ultraviolet-A radia- were placed in the light path in a plane conjugate to tion,13 the wavelength range was set at 320 to 600 nm, the retina. They divided the path into four beams with which encompasses all peak wavelengths of previous intensities of approximately 100%, 54%, 33%, and studies. As an experimental procedure, we chose to 17%. This filter set thus provided four simultaneous irradiate small patches of retina of anesthetized rats; irradiation levels in one exposure. Light reflected at advantages of this procedure are exact dosimetry and the fundus was directed by a mirror and lenses to the adjacent, unexposed, control retina. Funduscopy and observer's eye. In this way, the irradiated retinal field light microscopy were used for damage assessment, could be viewed. because these techniques can be performed relatively The output of this configuration was calibrated easily while they simultaneously allow for good com- every second experiment with a radiometer. The beam parison with data in the literature. had a maximum fall in irradiance of 25% toward the edges. Retinal irradiance was calculated from mea- sured irradiance according to the formula given by METHODS 5 Calkins et al,' with refraction index = 1.337 and dis- Animals tance from pupil to retina = 5.25 mm.16 The spectral transmission of rat ocular media was calculated from Male rats of the pigmented Long Evans strain were 17 13 obtained (Harlan CPB, Zeist, The Netherlands) when transmission data of rat cornea and lens. Radiation they were 30 days of age. They were subsequently kept losses in the other ocular media were neglected. The in a 12-hour light/12-hour dark cycle under 10 to 90 calculated spectral transmission is shown in Table 1. lux illumination. The animals used in experiments Table 1 also lists the bandwidth of the irradiations were 60 to 144 days old. Treatment of the animals according to the specifications of the menochromator. conformed to the ARVO Statement for the Use of The spectral characteristics of the irradiations were Animals in Ophthalmic and Vision Research. checked with a 512-diode array spectroradiometer. In addition, exposures were carried out at 488 Optics nm using an Argon ion laser (model 162A, Spectra- Optics were essentially the same as described by de Physics, Mountain View, CA) as the light source. The Lint et al.14 Briefly, a 450 W Xenon arc provided the optical configuration included a lens (f = 10) that radiation, which passed through a monochromator diverged the laser light beam, but for the rest, the (MM 12, Carl Zeiss, Oberkochen, Germany) and a optical setup was similar to the one described above. quartz lens to the rat eye, irradiating 18° X 13° of It provided irradiations with a similar field width. superior retina (Fig. 1). Maxwellian view conditions Irradiation were ensured because the quartz lens focused the Rats were sedated with ether and anesthetized by intra- monochromator's exit slit in the pupil plane of the peritoneal injection of pentobarbital (50 mg/kg body Downloaded from iovs.arvojournals.org on 10/02/2021 Two Spectral Types of Retinal Light Damage in Rat 853 TABLE l. Specification of Exposure Conditions for Funduscopic Threshold Damage Retinal Mean Funduscopic Wavelength Number of Transmittance Banduridth Itradiance Exposure Duration Threshold Dose (nm) Experiments Ocular Media* (nm) (mW/cm2) (range in minutes) (J/cm2) ± SEM 320 7 0.06 6 0.13 22-70 0.35 ± 0.09 340 4 0.28 5 0.66 15-25 0.79 ± 0.21 360 3 0.41 4 0.96 15-24 1.15 ± 0.25 380 13 0.52 5 1.76 8-23 1.37 ± 0.52 400 5 0.58 12 6.3 8-19 4.93 ± 1.22 420 6 0.60 11 8.3 60-70 31.5 ± 5.62 440 2 0.68 15 22.6 50-60 74.7 ± 9.6 470 7 0.72 19 46 134-285 577 ± 227 500 6 0.77 24 98 125-330 1145 ± 332 550 2 0.82 30 96 260-300 1612 ± 158 600 1 0.86 40 182 300 Subthreshold 1 Calculated from data on spectral transmittance of rat cornea" and lens.13 weight). An intravenous canula was applied to the tail, allowed to recover in the dark for 2 hours and was which ensured a constant intravenous infusion of pen- returned to the cage. tobarbital (15 mg/kg body weight per hour) and sa- line (1 ml/hour) during the experiment. Pupils were Analysis dilated with a drop of cyclopentolate HC1 1% and Three days after irradiation, the rat was sedated with phenylephrine HC1 5%. Atropine sulfate (0.3 ml of a ether and was anesthetized with an intraperitoneal solution of 0.5 mg/ml) was injected subcutaneously. injection of pentobarbital. Pupils were dilated as de- The rat was wrapped in an electric blanket and placed scribed above. The retina was inspected funduscopi- on a holder. Body temperature was maintained at cally by following the drawing of the retinal position 37.5°C to 38.5°C using a rectal thermometer coupled of the irradiation. to the electrical blanket. Eyelids were kept open with For histology, the rat was then transcardially per- adhesive tape.
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