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Effect of Three Different Sedatives on Electroretinography Recordings in Domestic Pigeons (Columba livia).

Abstract: This study was conducted to compare the effects of 3 different sedative agents on electroretinography (ERG) in domestic pigeons (Columba livia). Six pigeons were sedated with alfaxalone, xylazine, and medetomidine at separate times with a 1-week washout period between sedative administration. After sedation with each agent, pigeons underwent the modified ERG protocol adapted from the standardized protocol for dogs. The scotopic mixed rod and cone response was recorded after 20 minutes of dark adaptation, and the photopic cone response and photopic flicker response were recorded after 10 minutes of light adaptation. Either a 1-way analysis of variance or a Kruskall-Wallis test was used to compare the a-wave and b-wave implicit time and amplitude. No significant differences were observed in the scotopic mixed rod and cone response among all 3 sedatives used. Compared with alfaxalone, medetomidine significantly prolonged the a-wave implicit time, depressed the b-wave amplitude of photopic cone response, and prolonged the peak implicit time of the photopic flicker response (P < .05). These results show that medetomidine has a depressant effect on photopic ERG in pigeons at a dosage that produces light sedation.

Key words: electroretinography, alfaxalone, medetomidine, xylazine, sedation, avian pigeon, Columba livia

INTRODUCTION

In veterinary medicine, electroretinography (ERG) has been widely implemented for ophthalmologic examination, especially in small animals. It is considered a valuable and noninvasive method to evaluate retinal functions. These procedures range from investigating different types of retinal degeneration to routine examination before cataract surgery, each of them with different sets of protocols. (1-7) In exotic species, including birds, such protocols have not been established. (8) To date, results from reports of ERG performed in birds, especially those done in the clinical setting, (8-11) have been highly variable.

Many anatomic structures in a bird's eye are fundamentally different from those in a mammal's eye. Many factors, ranging from the shape of the globe to the size of the eye relative to the body weight to the existence of pecten, instead of retinal blood vessels, contribute to the differences in the clinical ophthalmology of birds compared with domestic animals, such as dogs. (12-14) Because a standardized ERG protocol for birds has not been established, any information on the technical aspect of ERG recording in birds is highly valuable, especially information that is practical and relevant to ERG clinical application, such as the effect of anesthetic drugs on ERG results. The use of anesthesia during ERG recording in animals has been generally recommended. (2,4,5) Although ERG recording without chemical restraint has been reported in several free-living raptors," (10) the use of chemical restraint agents helps to minimize artifacts resulting from involuntary muscle activity and to decrease the stress on birds. (8)

Many studies investigating different components of ERG in birds have mentioned using anesthetic agents. These have included sevoflurane in bald eagles (Haliaeetus leucocephalus) (8) isoflurane in Hispaniolan Amazon parrots (Amazona ventralis), scops owls (Otus scops), and little owls (Athene noctua) (9,11) U; chloral hydrate in the little owl (15); and a combination of ketamine, xylazine, and urethane in Japanese quail (Coturnix coturnix japonica). (16) However, these studies did not focus on the effect of anesthesia on the results of ERG recording. Therefore, those findings are of little value in interpreting the ERG results under the effect of an anesthetic agent during clinical examination.

Studies investigating the effects of different anesthetic agents on ERG recording in dogs showed that different agents exerted specific effects on the ERG recording. (17-19) Therefore, the anesthesia used in a clinical setting should be consistent, so the results obtained are comparable/ The purpose of this study was to compare the effects of 3 different sedative agents--alfaxalone, xylazine, and medetomidine--on ERG recordings in pigeons (Columba livia).

MATERIALS AND METHODS

This study was approved by the Seoul National University Institutional Animal Care and Use Committee (SNU-170210-1). Six domestic pigeons were used in this study. Three different sedative agents were administered to each bird, with a 1-week washout period between administration of each drug. The sedative agents used were alfaxalone (10 mg/kg), xylazine (10 mg/kg), and medetomidine (0.2 mg/kg). All drugs were injected intramuscularly in the pectoral muscle before the dark adaptation stage of ERG recording. After each injection, the pigeons were dark adapted for 20 minutes before ERG recording.

The ERG was recorded with a RETIport (Roland Consult Stasche & Finger GmbH, Brandenburg, Germany), with a goldring electrode 0.25 (3325RC; Roland Consult Stasche & Finger) used as the corneal electrode. Platinum subdermal needle electrodes (model F-E2, Astro-Med Inc, West Warwick, RI, USA) were used as the ground and reference electrodes. These electrodes were placed on the apex of the occiput subcutaneously and at approximately 0.3-0.5 cm lateral to the lateral canthus of the eye, respectively. Before ERG recording and before placing the corneal electrode, proparacaine hydrochloride eye drops were applied to the cornea as a topical anesthetic. In all pigeons, the ERG was recorded from the right eye only.

Three ERG recordings, adapted from the guidelines of ERG recording in dogs/ were performed: 1) scotopic (dim-light) mixed rod and cone response, 2) photopic (bright light) cone response, and 3) photopic flicker response. A single, mixed rod and cone response was obtained at a stimulus intensity of 3.0 cd s/[m.sup.2]. For photopic cone function, 4 flashes at a frequency of 4.9 Hz presented at the same stimulus intensity were obtained. For the flicker response, 8 flashes were presented at a frequency of 31.25 Hz. The scotopic mixed rod and cone response was recorded after 20 minutes of dark adaptation. The pigeons were then light adapted for 10 minutes by using a background light of 30 cd/[m.sup.2]. The photopic cone response, followed by the flicker response, was then recorded.

Statistical analyses

For the scotopic mixed rod and cone and photopic cone responses, the data obtained were the a-wave and b-wave implicit time and amplitude. For the photopic flicker response, the data obtained were the peak implicit time and the b-wave amplitude. Statistical analysis of data was performed with SPSS Statistics 23.0 (IBM Corp, Armonk, NY, USA). A 1-way analysis of variance was performed to compare the data among the 3 sedatives, except for the data of b-wave implicit time from the photopic cone response, which were tested with the Kruskall-Wallis test. Results were considered significant at P < .05.

RESULTS

The ERG results of scotopic mixed rod and cone responses under the influence of all the drugs used showed a distinct a-wave, which was a negative deflection followed by an ascending slope leading to the positive deflection of the b-wave (Fig 1). Between the a-wave and b-wave, the oscillatory potential (OP) superimposed at the ascending slope was observed during the scotopic response (Fig 1) but was absent during the photopic cone response (Fig 2). In the scotopic response result, a small positive deflection was sometimes observed before the negative a-wave, which was a stimulus artifact driven by the introduction of a brief white-flash stimulus (Fig 1). (2) In the photopic flicker response, a series of distinctive waves were observed, which showed that the pigeon's retina was able to respond to the individual flashes presented at a frequency of 31.25 Hz (Fig 3). The b-wave amplitudes of the photopic cone and photopic flicker responses were, in general, lower than those of the b-wave amplitudes of the scotopic mixed rod and cone response for all 3 sedatives (Tables 1-3).

For the scotopic mixed rod and cone response, no significant differences were observed in any of the ERG components for all of the drugs used. For the photopic cone response, significant differences were observed in the a-wave implicit time (Z' = .01) and b-wave amplitude (P = .015) between alfaxalone and medetomidine. Compared with alfaxalone, medetomidine significantly prolonged the awave implicit time by 3.28 ms and depressed the fawave amplitude by 55.55 pV. For the photopic flicker response, a significant difference was observed in the implicit time (P = .03), which also occurred between alfaxalone and medetomidine. In addition, medetomidine significantly prolonged the implicit time by 4.91 ms. Compared with alfaxalone or medetomidine, xylazine showed no significant difference in any of the ERG recordings.

DISCUSSION

The results of this study showed that the amplitudes of b-waves were significantly higher with alfaxalone sedation than it was with medetomidine sedation. These results suggest that alfaxalone could be a better option than medetomidine and, to a lesser extent, xylazine for sedation during ERG recording in pigeons.

During the scotopic response of the pigeon ERGs in this study, OP was observed under all 3 sedatives. This is an inhibitory circuit driven by amacrine cells, whose appearance and numbers vary among individuals and species. This circuit is highly dependent on retinal circulation and is reduced in the event of retinal ischemia; therefore, its use has been indicated in the diagnosis of some retinal diseases. (2) Although special adaptation levels and filtering techniques are required to maximize OP recording, OPs are sometimes shown during general protocols used to record a-waves and b-waves. However, they are small and sometimes difficult to discern among the major components of the ERG. (20) Previous ERG studies in Hispaniolan Amazon parrots, and several species of raptors demonstrated OPs during scotopic ERG recordings. (9,10)

The amplitude gained during the photopic cone response is expectedly lower than that of the scotopic mixed rod and cone response. (3) This might be caused by a different sensitivity between the rod and cone photoreceptors to the light. Rods are known to be very sensitive to light. They can detect individual quanta of light resulting in a tremendous increase in signal gained during the phototransduction. (21) This explains the higher amplitude gained during the scotopic response in which both rod and cone photoreceptors were active.

The scotopic responses to a stimulus intensity of 3.0 cd s/[m.sup.2] in this study were relatively low in amplitude compared with those of a previous study on several species of raptors. These species included the Cooper's hawk (Accipiter cooperii), red-tailed hawk (Buteo jamaicensis), American kestrel (Falco sparverius), turkey vulture (Catlwrtes aura), great horned owl (Bubo virginianus), barred owl (Strix varia), and eastern screech owl (Megascops asio). (10) The different results obtained in the raptor study may have been a result of a different ERG machine, different corneal electrodes used, or the absence of anesthesia, as well as species differences. Results of 2 other ERG studies from the same institution on bald eagles and Hispaniolan Amazon parrots revealed that the amplitudes from the eagles were substantially higher than those from the parrots. This result was despite both studies using the same protocols and being performed under the same anesthetic agent. (8,9)

The 3 drugs used in this study represented 2 different types of anesthetic agents that act on 2 different receptors. Alfaxalone is a [GABA.sub.A] receptor agonist, whereas xylazine and medetomidine are both oci-adrenoceptor agonists. (22,23) The active enantiomer of medetomidine--dexmedetomidine--exhibits a more-selective binding affinity to [[alpha].sub.2]:[[alpha].sub.1] receptor, at a ratio of 1620:1, than does xylazine. Xylazine has a selective binding affinity of only 160:1; therefore, medetomidine has the more-profound sedative effect. (24) The stronger character of medetomidine over xylazine might explain its suppressing effect when compared with alfaxalone, despite these drugs acting on different receptors. In contrast, xylazine, being a relatively weak drug, showed no significant differences compared with alfaxalone and medetomidine.

Results of a study in dogs also showed that medetomidine had a depressant effect on ERG recording. (19) Medetomidine is known to significantly prolong the a-wave and b-wave implicit times and to depress the amplitude of both waves on the scotopic response from 3.0 cd s/[m.sup.2] light intensity. Compared with results of that previous study in dogs, we observed some differences in our results regarding the depressant effect of medetomidine. First, the study in dogs was conducted in scotopic conditions; in our study, in pigeons, the effect was observed only in the photopic condition. Second, despite the difference in light adaptation, the overall effect of medetomidine on the ERG components in our study was minimal, with only the prolongation of the a-wave implicit time and depression of the b-wave amplitude observed. The differences in the ratio of rod versus cone composition of the retina between dogs and pigeons might be the reason for this different observation; dogs have a rod-rich retina, whereas pigeons have a cone-rich retina. (25-27) In the scotopic condition, the flash intensity of 3.0 cd s/ [m.sup.2] should stimulate both the rod and cone photoreceptor systems; however, the main response would still be derived from the rod system. In general, the greater the number of photoreceptor cells being stimulated or activated, the greater the generated amplitude is. (28) Because pigeons have cone-rich retinae with fewer rod cells, their retinae might generate a much lower ERG response during the scotopic response relative to that shown by the retinae in dogs. Hence, the amplitude differences across the 3 drugs in the scotopic response in our study were not significantly different, as was seen in dogs.

Another possible explanation for the different results in this study of pigeons compared with those studies in dogs could be the sedation levels in both studies. In the present study, medetomidine was administered via intramuscular injection, whereas in the study on dogs, it was administered intravenously. This difference in administration routes might have limited the bioavailability of medetomidine. In addition, results of a previous study in pigeons suggested that medetomidine may have a lower affinity to avian [[alpha].sub.2]-adrenoceptors than to mammalian [[alpha].sub.2]-adrenoceptors. Therefore, a higher medetomidine dose of 2 mg/kg may result in less sedation in pigeons than would a dose of 80 [micro]g/kg in dogs. (29)

The dose of drugs used in this study was based on those recommended or commonly used in pigeons by practitioners. (30) These doses mostly produced light sedation, with the pigeons appearing calm but not fully immobilized. The sedation levels produced by the 3 drugs were generally adequate to facilitate the ERG recording throughout the procedure. However, ERG recording in agile pigeons is difficult because they still struggle when restrained, even with sedation. One disadvantage of injected anesthetics is that their effects vary according to dose and individual responses. Despite these disadvantages, injectable anesthetics are used in birds, especially when inhalation anesthetics are unavailable. (31)

Considering that the pharmacokinetics among species of birds is highly varied, the data obtained from pigeons might not be directly transferable to other bird species. However, these data may be better extrapolated than are data from mammalian species. (31) Therefore, this study could provide better information on how these injectable anesthetics will affect ERG recording in avian species than would information obtained from mammalian species, such as dogs.

Furthermore, the bird retina is different from the mammalian retina. Not only is the rod-to-cone ratio different, but the structures and types of photoreceptors are also different. Birds have a double cone and possess oil droplets in the distal ellipsoid region of the inner segment. (26,32) Birds also have more varied visual pigments in the cone photoreceptors, with pigeons having at least 4 types of visual pigments compared with 2 types in dogs. (25,26,32) All of these differences could contribute to the variations in the ERG result.

Birds are highly dependent on their visual system, especially in conjunction with their flying behavior. (14) Therefore, a bird's eye has a high temporal resolution. The ability of the avian eye to process temporally varying stimuli at a certain speed can be determined by the flicker-fusion frequency test. This test measures the frequency at which an individual can no longer resolve the stimuli of flickering light. The flickering light will then appear as a continuous light, and that frequency is referred to as the critical flicker-fusion frequency. Pigeons, in particular, are known to have the highest critical flicker-fusion frequency reported for a vertebrate, 143 Hz. (33) In this study, the photopic flicker presented at a flash intensity of 3.0 cd s/[m.sup.2] and at a frequency of 31.25 Hz, which is a frequency that can still be resolved by pigeons. For this photopic flicker response, medetomidine prolonged the implicit time when compared with alfaxalone.

A limitation of this study was the inability to induce mydriasis during ERG recordings. Generally, ERG recording should be performed in the mydriatic pupil to ensure an even distribution of light to the retina. (5) However, many recent studies of clinical ERG in several avian species were performed without the use of mydriatic agents. (8,9,11) The avian iris musculature consists of striated muscle fibers, which are insensitive to general mydriatic agents. Instead of parasympatholytics and sympathomimetics, nondepolarizing muscle relaxants, such as d-tubocurarine solution, have been suggested for use in dilating a bird's pupil. This can be done through intracameral injection or topical instillation. (16,34) However, results of 1 study in pigeons showed that topical instillation of d-tubocurarine was not as effective as intracameral injection in dilating the pupil." Intracameral injection of a mydriatic agent for clinical examination was not an option in this study because it carries a risk of complications, such as infection and cataract formation. (35) Therefore, the use of mydriatic agents was omitted in this study.

Further study is required to investigate the effectiveness of topical mydriatic drugs in pigeons. Rocuronium bromide has recently been reported to dilate the pupil of orange-winged parrots (Amazona amazonica) (36) and several other species of birds, including Hispaniolan Amazon parrots, (37,38) tawny owls (Strix aluco), (39) common buzzards (Buteo buteo), little owls, (40) and European kestrels (Falco tinnunculus). (41) Electroretinography recording on a dilated pupil might produce a maximum amplitude and, therefore, provide a better way to investigate retinal function in birds.

Under alfaxalone sedation, the amplitudes of fawaves were significantly higher than those under medetomidine sedation. This suggests that alfaxalone could be a better option than medetomidine and, to a lesser extent, xylazine for ERG recording in pigeons.

Acknowledgments: The scholarship for LS was provided by the Indonesian Endowment Fund for Education (LPDP), Ministry of Finance, Indonesia. This study was supported through the BK21 PLUS Program for Creative Veterinary Science Research and the Research Institute for Veterinary Science of Seoul National University, Seoul, Korea.

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Lina Susanti, DVM, MS, Seonmi Kang, DVM, MS, PhD, Sangwan Park, DVM, PhD, Eunjin Park, DVM, Yoonji Park, DVM, Boyun Kim, DVM, Sunhyo Kim, DVM, and Kangmoon Seo, DVM, MS, PhD, Dipl AiCVO

From the Department of Veterinary Clinical Sciences, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, 1 Gwanak-Ro, Gwanak-Gu, Seoul, 08826, Korea.

Caption: Figure 1. Representative results of the scotopic mixed rod and cone response of pigeons sedated using 3 different anesthetic agents: (A) alfaxalone, (B) xylazine, and (C) medetomidine. The (a) identifies the a-wave, and the (b) identifies the b-wave. The oscillatory potential is visible between the a-waves and b-waves (arrows). The (N) indicates the presentation of light stimulation. A small, positive deflection before the negative a-wave was a stimulus artifact driven by the introduction of a brief white-flash stimulus (asterisk).

Caption: Figure 2. Representative results of the photopic cone response of pigeons sedated using 3 different anesthetic agents: (A) alfaxalone, (B) xylazine, and (C) medetomidine. The (a) identifies the a-wave, and the (b) identifies the b-wave. The (N) indicates the presentation of light stimulation. Only the a-waves and b-waves are visible.

Caption: Figure 3. Representative results of the photopic flicker response of pigeons sedated using 3 different anesthetic agents: (A) alfaxalone, (B) xylazine, and (C) medetomidine. The vertical bars indicate the presentation of the light stimulations (the first presentation denoted as Nl). PI represents the first peak/amplitude.
Table 1. Descriptive statistics of the scotopic mixed rod and
cone electroretinography response in pigeons.

               Scotopic mixed rod and cone response (a)

               Implicit time, ms

Drug           a-wave                 b-wave

Alfaxalone     14.03 [+ or -] 1.58    39.03 [+ or -] 11.04
Xylazine       16. 56 [+ or -] 2.57   39.66 [+ or -] 7.93
Medetomidine   12.48 [+ or -] 2.18    41.51 [+ or -] 8.53

               Amplitude, [micro]V

Drug           a-wave                 b-wave

Alfaxalone     56.51 [+ or -] 17.88   185.54 [+ or -] 82.53
Xylazine       62.38 [+ or -] 18.00   161.38 [+ or -] 54.66
Medetomidine   38.78 [+ or -] 17.41   161.34 [+ or -] 66.38

(a) Mean [+ or -] SD.

Table 2. Descriptive statistics of the photopic cone
electroretinography response in pigeons.

               Photopic cone rcsponse (a,b)

               Implicit time, ms

Drug           a-wave                     b-wave

Alfaxalone     11.28 [+ or -] 2.31 (A)    28.86 [+ or -] 3.73
Xylazine       14.85 [+ or -] 2.44 (AB)   34.50 [+ or -] 5.91
Medetomidine   14.56 [+ or -] 2.28 (B)    33.00 [+ or -] 2.23

               Amplitude, [micro]V

Drug           a-wave                 b-wave

Alfaxalone     29.26 [+ or -] 9.46    156.81 [+ or -] 61.93 (A)
Xylazine       26.73 [+ or -] 6.61    91.95 [+ or -] 25.02 (AB)
Medetomidine   25.20 [+ or -] 11.07   101.25 [+ or -] 44.99 (B)

(a) Mean [+ or -] SD.

(b) Means in the same column with different letters are
significantly different (P < .05).

Table 3. Descriptive statistics of the photopic flicker
electroretinography response in pigeons.

                Photopic flicker response (a)

Drug            Implicit time, ms          Amplitude, [micro]V

Alfaxalone      23.40 [+ or -] 1.26 (A)    122.33 [+ or -] 46.33
Xylazine        28.81 [+ or -] 4.35 (AB)   73.65 [+ or -] 26.07
Medetomidine    28.31 [+ or -] 2.78 (B)    89.81 [+ or -] 46.07

(a) Mean [+ or -] SD.

(b) Means in the same column with different letters are significantly
different (P < .05).
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Title Annotation:Original Study
Author:Susanti, Lina; Kang, Seonmi; Park, Sangwan; Park, Eunjin; Park, Yoonji; Kim, Boyun; Kim, Sunhyo; Seo
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Jun 1, 2019
Words:4769
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