Electroretinography in the western gray kangaroo (macropus fuliginosus)

Veterinary Ophthalmology (2010) 13, Supplement 1, 41–46 Electroretinography in the western gray kangaroo(Macropus fuliginosus) Amber L. Labelle,* Ralph E. Hamor,* Kristina Narfstro¨m† and Carrie B. Breaux*,1*Department of Veterinary Clinical Medicine, Veterinary Teaching Hospital, Urbana, Illinois; †Ruth M Kraeuchi Endowed Professor Emeritus of VeterinaryOphthalmology, Columbia, Missouri Objective To perform electroretinography on normal anesthetized western graykangaroos (Macropus fuliginosus).
Animals studied Six captive western gray kangaroos.
Procedures The kangaroos were anesthetized using a combination of ketamine andmedetomidine via a remote drug delivery system, then were maintained on isoflurane after endotracheal intubation and reversal of the medetomidine with atipamazole.
Animal Emergency andSpecialty Center, 5019 N.
After a minimum of 20 min of dark adaptation, electroretinograms were obtained using a handheld electroretinography (ERG) machine using a single flash protocol at three light intensities: 10 mcd.s/m2, 3000 mcd.s/m2, 10 000 mcd.s/m2.
Results At 10 mcd.s/m2 the mean b-wave amplitude and implicit time was 102.0 lV(SD ± 41.3 and 95% CI 68.9–135.1) and 78.4 ms (SD ± 8.3 and 95% CI 71.8–85.0).
At 3000 mcd.s/m2 the mean a-wave amplitude and implicit time was 69.9 lV(SD ± 20.5 and 95% CI 53.5–86.3) and 17.6 ms (SD ± 1.5 and 95% CI 16.4–18.8)and the mean b-wave amplitude and implicit time was 175.4 lV (SD ± 35.9 and 95%CI 146.7–204.1) and 74.1 ms (SD ± 3.5 and 95% CI 71.2–76.9). At 10 000 mcd.s/m2the mean a-wave amplitude and implicit time was 89.1 lV (SD ± 27.1 and 95% CI67.5–110.8) and 16.8 ms (SD ± 1.0 and 95% CI 16.0–17.0) and the mean b-waveamplitude and implicit time was 203.7 lV (SD ± 41.4 and 95% CI 170.6–236.8) and75.4 ms (SD ± 3.3 and 95% CI 72.8–78.1).
Conclusion Electroretinography outside of the typical clinical setting is feasible using aportable ERG system and allows for quick analysis of retinal function in exoticspecies.
Key Words: electroretinogram, eye, macropod, Macropus fuliginosus, retina, westerngray kangaroo a-wave is produced by the hyperpolarization of photorecep- tors as they undergo phototransduction, whereas the b-wave Electroretinography (ERG) is commonly utilized in veteri- is produced primarily by bipolar cells.6–8 Traditional ERG nary ophthalmology to assess and document retinal electri- units are bulky and nonportable, however within the last cal function. The first reports of canine and feline ERGs 10 years several portable ERG systems have become com- occurred in the early and mid 20th century.1–3 ERG is used mercially available, making electrodiagnostic assessment of in research settings for the study of inherited and acquired nontraditional patients possible outside of the traditional retinopathies, in clinical settings for differentiating retinal research laboratory or clinical setting.
vs. central nervous system disease in cases of acute vision loss Western gray kangaroos (Macropus fuliginosus) are macro- and for evaluating retinal electrical function in patients with pods native to Southwestern Australia. With weights from opaque ocular media that precludes direct examination of 28 to 54 kg, heights up to 1.1 m, and tail lengths from 80 to the posterior segment.4,5 The ERG represents a complex 100 cm, they are one of the largest species of kangaroo.
summation of electrical potentials and currents generated Males are generally twice as large as females, however they within the cells of the retina. The negative deflection of the are all herbivorous. Although western gray kangaroos are Ó 2010 American College of Veterinary Ophthalmologists commonly housed in zoological collections, there is a then blindly intubated using a 6.0 or 7.0 mm internal diame- paucity of information about the normal ophthalmic ter endotracheal tube, and isoflurane was continuously examination findings and common ocular diseases of this administered at concentration of 1–3% with 2–3 L/min of species. Published reports include a review of common mar- oxygen. Atipamazole (Antisedan; Pfizer Animal Health) was supial ocular diseases, a single report of retinal degeneration then administered intramuscularly at a dose of five times that in a Goodfellow’s tree kangaroo (Dendrolagus goodfellowii) of the previously administered medetomidine, and the kan- and several detailed descriptions of a viral outbreak of ante- garoo was maintained on isoflurane during the ERG. The rior uveitis, chorioretinitis, optic neuritis and encephalitis amount of time between administration of the atipamazole causing vision loss in Australian kangaroos.9–13 A review of and the start of the ERG varied from 10 to 16 min.
normal ocular examination findings in a captive mob of wes- Atipamazole is reported to reverse sedation and analgesia in dogs within 5–10 min, and these effects are extrapolated in A retrospective evaluation of necropsy data on kangaroos western gray kangaroos as no pharmacologic studies are housed in a single zoological collection revealed a high prev- available in this species.18 After conclusion of the ERG alence of histologic lesions compatible with hypertension, and all additional anesthetic monitoring, administration of including renal arteriolar smooth muscle hypertrophy, isoflurane and oxygen was discontinued and the kangaroos extracellular matrix accumulation within renal arterioles, were moved to a dark and quiet recovery area where renal vascular tortuosity, juxtaglomerular hyperplasia and extubation was performed at the first sign of swallowing or hypertrophy of arterioles and arteries in both the retina and purposeful movement. No regurgitation or vomiting was central nervous system.15 Hypertension is frequently associ- ated with retinopathy, particularly in the cat.16 A recent Each kangaroo in this study had received a complete oph- report identified decreased b-wave amplitudes in spontane- thalmic examination under general anesthesia 3 months ously hypertensive rats.17 Establishing a protocol for ERGs prior to this study. Complete ophthalmic examination in western gray kangaroos may be a useful part of evaluating included diffuse illumination, slit lamp biomicroscopy a mob for hypertension and its associated ocular lesions.
(Kowa-SL2; Kowa, Tokyo, Japan), and indirect funduscopy The goal of this study was to demonstrate a method for per- (Keeler Instruments Inc., Broomall, PA, USA) with a 2.2D forming ERGs in an exotic species in a nonclinical setting.
handheld condensing lens (PanRetinal 2.2; Volk Optical,Inc., Mentor, OH, USA). Intraocular pressure (IOP) wasestimated using rebound (Tonovet; Icare Finland Oy, Espoo, Finland) and applanation tonometry (Tonopen-XL; The study protocol was approved by the Brookfield Zoo Research and Scientific Committee and Institutional Animal No ophthalmic abnormalities were observed in any kan- Care and Use Committee. A mob of six captive adult wes- garoo included in the ERG study group that could poten- tern gray kangaroos (three males and three females) were tially impact the ERG. Observed abnormalities did include a included in the study, ranging in age from 3 to 7 years and in subepithelial scar, incipient anterior cortical cataract, eyelid weight from 22.4 to 67.5 kg. All kangaroos were considered notch defect, nuclear sclerosis and vitreal degeneration. One to be in good health at the time of the study with no evidence kangaroo in the mob was observed to have a regional focal of visual deficits. Each kangaroo was anesthetized using a choroidal hypoplasia and an optic nerve coloboma, however remote drug delivery system (Telinject; Telinject USA, Inc., that kangaroo was not included in this study.14 Agua Dulce, CA, USA) with 2 mg/kg ketamine hydrochlo- Since all kangaroos had been examined 3 months prior to ride (Ketaset; Fort Dodge Animal Health, Fort Dodge, IA, this study, complete ophthalmic examination was not per- USA) and 50 lg/kg medetomidine hydrochloride (Domitor; formed prior to the harvesting of ERGs in this study to avoid Pfizer Animal Health, Exton, PA, USA) administered intra- the deleterious effects of excessive light exposure on the muscularly with doses based on the most recently available ERG.19 Tonometry with applanation and rebound tonome- body weight of the animal (information no older than try was performed prior to the instillation of tropicamide 3 months for any kangaroo). The anesthetic drugs were 1% solution (Tropicamide 1% USP; Alcon Laboratories, administered within the kangaroo enclosure while the ani- Inc., Fort Worth, TX, USA) for mydriasis. Dark adaptation mals were free-ranging, and when the kangaroo became times varied from 20 to 60 min prior to beginning ERG.
recumbent and immobilized, it was transferred to a building Since complete darkness was not possible for the entirety of within the kangaroo enclosure. Each kangaroo was carefully the time of dark adaptation due to the need for continued monitored while under anesthesia, including heart rate and anesthetic monitoring and the complex intubation process, rhythm, direct and indirect blood pressure, arterial oxygen dark adaptation was achieved by using adhesive tape to close saturation and respiratory rate. After obtaining direct and the eyelids of each kangaroo and then taping a patch of dark indirect blood pressure measurements as part of an unre- material over the eyelids to simulate a dark environment.
lated study, each kangaroo was administered 5% isoflurane This technique allowed for the necessary pre-ERG dark (Isoflo; Abbott Animal Health, Abbott Park, IL, USA) by adaptation without interfering with the work of the facemask with oxygen at 2–3 L/min. Each kangaroo was anesthetic team and monitoring. After dark adaptation was Ó 2010 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 13, 41–46 e l e c t r o r e t i n o g r a p h y i n t h e w e s t e r n g r a y k a n g a r o o 4 3 concluded (minimum of 20 min), the ERG was performed using a monopolar electrode-contact lens (ERG-jet; NicoletInstruments, Madison, WI, USA) applied to the cornea with hypromellose 2.5% gel as a coupling agent (Gonak; Akorn,Inc., Buffalo Grove, IL, USA), male subdermal platinum needle electrodes (FD-E2-24; Astro-Medical, Inc. Warwick,RI, USA) and a portable ERG machine, the Handheld Multispecies ERG (HMsERG) (HMsERG Model 1000; RetVetCorp, Columbia, MO, USA). The ground electrode needle was placed at the apex of the occiput directly betweenthe two ears, and the reference needle was placed approxi- mately 2 cm lateral to the lateral canthus of the eye being 0 10 20 30 40 50 60 70 80 90 100
The Quick Ret Check protocol was used in both eyes Figure 1. Scatter plot of the 10 mcd.s/m2 ERG b-wave values. At this of all kangaroos. The Quick Ret Check Protocol, which low light intensity, no a-wave values are recorded.
is part of the software of the HMsERG unit, was devel-oped by Dr. Kristina Narfstro¨m. The HMsERG unit uti- lizes a white flash within a mini-Ganzfeld for stimulationof the retina. It utilizes only three levels of light stimuli All kangaroos had normal ocular examinations at the time of in order to obtain an overall evaluation of retinal function ERG. Mean IOP as estimated with applanation tonometry very quickly with variable flash durations of 0.005–5 ms, was 12.9 mmHg with SD ± 10.5 mmHg and a range of depending on the test protocol. The first set consists of 9–20 mmHg. Mean IOP as estimated with rebound tonom- the average response to four light flashes (2 s in between etry was 10.1 with SD ± 4.8 mmHg and a range of flashes) at 10 mcd.s/m2, followed by a single flash at 7–19.5 mmHg. Bilateral ERGs were obtained from all six 3000 mcd.s/m2 and, after 20 s, another single flash at kangaroos, however in two kangaroos (one male and one 10 000 mcd.s/m2.20 In dark adapted conditions ‘pure’ rod female), the reading in one eye was uninterpretable. All responses are obtained through the first set of low light kangaroos were normotensive, normothermic and neither intensity flashes, while for the second and third flash hypoxemic nor hypercapneic at the time of ERG harvesting.
stimuli, the responses are derived from a mixture of rod At 10 mcd.s/m2 the mean b-wave amplitude and implicit and cone photoreceptors. The bandpass of the HMsERG times were 102.0 lV (SD ± 41.3 and 95% CI 68.9–135.1) and 78.4 ms (SD ± 8.3 and 95% CI 71.8–85.0) (Fig. 1). No During the ERG, all ambient lights were turned off with a-wave is obtained in this low amplitude ERG response, the exception of anesthetic monitoring equipment monitors, which only consists of a low amplitude and late-onset b- which remained on but were positioned away from the kan- wave, for which amplitude and implicit time data is reported.
garoo’s head, and a single 20 watt red light which was used At 3000 mcd.s/m2 the mean a-wave amplitudes and implicit to illuminate the kangaroo’s head and the ERG equipment.
times were 69.9 lV (SD ± 20.5 and 95% CI 53.5–86.3) and Ambient light intensity was not measured. The room in 17.6 ms (SD ± 1.5 and 95% CI 16.4–18.8) and the mean which all ERGs were performed was not insulated in any b-wave amplitude and implicit times were 175.4 lV way from external electrical interference. Both cellular tele- (SD ± 35.9 and 95% CI 146.7–204.1) and 74.1 ms phones and laptop computers were present within the exam- (SD ± 3.5 and 95% CI 71.2–76.9) (Fig. 2). At 10 000 mcd.s/ ination room. At the conclusion of ERG, each kangaroo m2 the mean a-wave amplitude and implicit times and received a brief anterior segment examination using diffuse amplitudes were 89.1 lV (SD ± 27.1 and 95% CI illumination and indirect funduscopy using a 2.2D condens- 67.5–110.8) and 16.8 ms (SD ± 1.0 and 95% CI 16.0–17.0) ing hand lens to ensure that no new ophthalmic lesions had and the mean b-wave amplitude and implicit times were developed since the previous examination 3 months prior to 203.7 lV (SD ± 41.4 and 95% CI 170.6–236.8) and 75.4 ms (SD ± 3.3 and 95% CI 72.8–78.1) (Fig. 3). The normal All ERGs were analyzed using the HMSERG software, ERG of kangaroo #6 is presented as Fig. 4.
and a-wave and b-wave amplitudes and implicit times wererecorded for each kangaroo. For the four kangaroos in which bilateral ERGs were obtained the data from the left andright eyes were combined and averaged for a single reading.
This report demonstrates a practical method of performing The limited data set precluded inferential statistical testing, ERG on an exotic species. ERG has not previously been so mean, standard deviation (SD) and 95% confidence inter- reported in the western gray kangaroo, however one report val (CI) with alpha = 0.05 were reported for the amplitudes details the ERG findings and photoreceptor spectral and implicit times of each ERG (Excel; Microsoft, Inc., sensitivities of a related macropod, the tammar wallaby (Macropus eugenii).21 Veterinary ERG has a wide variety of Ó 2010 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 13, 41–46 Kangaroos as a species are reported to be affected with nutri-tional cataracts, so establishing reference values of normal ERGs may be of significant diagnostic value.13 Electroretinography is plagued by a myriad of factors that interfere with accurate and reliable recordings of good qual-ity. Such factors include excessive ambient electrical noise, inappropriate placement of ground and reference electrodes, faulty electrodes, poor contact between the corneal surface and the active electrode, irrelevant physiologic activity andinappropriate or faulty filters and amplifiers.29 In this study, ERGs were unable to be obtained from one eye of two kan- 0 10 20 30 40 50 60 70 80 90
garoos. Although wide variety of physiologic, pathologic and pharmacologic factors also influence the ERG, includ-ing body temperature, oxygenation/ventilation status, IOP, Figure 2. Scatter plot of the 3000 mcd.s/m2 ERG values. The clus- and sedatives/anesthetics, these parameters were carefully tered values to the left represent a-wave values while the clustered valuesto the right represent b-wave values.
monitored and are considered unlikely to have contributedto the poor ERG recordings.30 Faulty electrodes and wiringare possible contributors to the poor ERG recordings, how- ever the electrodes and wiring were successfully utilized for subsequent recordings, thus making this cause less likely.
Excessive external electrical interference was considered a possible cause of the uninterpretable waveforms, however the electrical interference within the room (from external power cords and other electrical equipment) remained con- stant during the recording period, making this less likely. Amore likely possibility is poor positioning of the reference electrode, causing amplification of background physiologicnoise or poor contact between the JET electrode and the 0 10 20 30 40 50 60 70 80 90
cornea. A possible improvement of the technique presented here would be to reposition reference electrodes when poorrecordings were obtained, liberal application of the coupling Figure 3. Scatter plot of the 10 000 mcd.s/m2 ERG values. The clus- media between the electrode and the cornea and minimiza- tered values to the left represent a-wave values while the clustered values tion of the amount of ambient electrical interference by to the right represent b-wave values.
turning off unnecessary electrical devices. Future studiesmay investigate alternative corneal electrodes, including a applications, from the pre-operative screening of patients microfiber electrode, that may be more appropriate for the with mature cataracts prior to cataract surgery to complex curvature and size of the kangaroo cornea.31 diagnostic protocols for detecting subtle changes in rod/ In both human and veterinary ophthalmology, there has cone function in hereditary retinal degenerations. Although been a call for standards of uniformity in electrodiagnostic various research and clinical screening protocols have been testing of retinal function, an attempt to make results from well described, there is a paucity of information regarding different laboratories or clinics more comparable.20,32 The ERG in exotic species. The size and bulk of most ERG protocol utilized in the study is modeled after the guidelines machines have historically limited their field applications suggested in these consensus statements, however it differs and use in exotic species that could not be examined in a hos- from longer and more elaborate protocols in that it is meant pital setting. With the development of a hand-held ERG to be a fast screening test and does not give detailed and machine such as the HMsERG, the feasibility of performing complete information about rod and cone function sepa- ERG in exotic species housed in zoological collections has rately. Cone function tests were not performed in this study because of time limitations with other phases of the study.
As phacoemulsification in exotic species has become more The major advantage to the QuickRetCheck protocol used common, so does the need for accurate and accessible in this study is its brevity, which is ideal for use under field ERG.22–28 The purpose of this study was to describe a suc- research or clinical conditions. The protocol has previously cessful technique for field ERG in western gray kangaroos, been utilized in dogs but has not been described in other however the technique has applications to a wide variety of species.33 Other possible protocols that could be utilized exotic species, particularly those for which capture and that may have the same advantage of brevity include the transportation to a hospital for pre-operative evaluation is shorter gross retinal function protocol proposed for use in either not feasible or not in the best interest of the animal.
Ó 2010 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 13, 41–46 e l e c t r o r e t i n o g r a p h y i n t h e w e s t e r n g r a y k a n g a r o o 4 5 Figure 4. Representative recordings using theQuickRetCheck protocol in a 7-year-old westerngray kangaroo. Bilateral recordings are shown withtracings from OS on the left side and tracings fromOD on the right. For evaluation of the rod system(in the dark adapted state) the average of four flashesof low intensity light stimulation (10 cd.s/m2) isused, followed by two single flashes of high intensitylight stimulation, one flash at 3 cd.s/m2 and anotherat 10 cd.s/m2. The latter two light stimuli showresponses of mixed rod and cone photoreceptors.
The role of general anesthesia and its affect on the ERG described in the western gray kangaroo, however in the is important for the accurate interpretation of the ERG.
dog, the average duration of action for medetomidine in Medetomidine is reported to significantly but minimally the dog is approximately 30 min, and 20 min for keta- prolong the implicit times and decreases the amplitudes of mine.37 It is less likely that either ketamine, given its dura- the canine ERG as evaluated using the HMsERG.33 The tion of action, or medetomidine, given its duration of inhalant anesthetic gas isoflurane has been demonstrated action and the administration of atipamazole as a reversal to decrease the amplitudes of the a and b-waves compared agent, significantly impacted the ERG, and therefore to sedation with tiletamine-zolazepam in normal dark- isoflurane is likely the largest influence on the ERG out- adapted dogs, as have the inhalant gasses sevoflurane and come in this group of anesthetized kangaroos. The implicit halothane.34,35 The combination of thiopental and isoflura- times of the b-wave at all light intensities were markedly ne has been shown to decrease the implicit time and ampli- increased compared to the identical ERG protocol with tude of the a wave in normal dogs compared to the the HMsERG machine in dogs sedated with only mede- combinations of medetomidine and ketamine or xylazine tomidine, which may represent a drug effect or normal and ketamine.36 The anesthesia protocol in this case was physiology for this exotic species.33 It would be extremely selected as part of a related study on the affects of two anes- difficult to perform an ERG in a nonanesthetized adult thetic protocols on the blood pressure of western gray kan- kangaroo due to their size and temperament, therefore the garoos. Medetomidine, an alpha-2-agonist and ketamine, a results of this study in anesthetized kangaroos provide a centrally acting N-methyl-D-aspartic acid receptor-inhibi- reasonable reference range for ERG values at three light tor, are a commonly used combination for immobilization of intensities using a field ERG protocol. This study provides western gray kangaroos. Since medetomidine is reported to evidence that ERGs can be successfully performed in the cause peripheral hypertension in dogs, atipamazole was zoological species using a portable ERG unit and an ERG administered to the kangaroos in this study after beginning protocol adapted for field purposes, opening up new insufflation with isoflurane to eliminate this potentially avenues for future research in retinal electrophysiology.
confounding affect on measurement of blood pressure.
The average time from administration of the ketamine/ medetomidine to the beginning of the ERG was 64.2 minwith a range of 40–83 min. The pharmacokinetics of the The authors gratefully acknowledge Dr. Hsin-Yi Weng for anesthetic agents used in this study have not been well her contribution to the statistical analysis.
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