Mydriasis is crucial in ophthalmology because it enables ophthalmoscopy and surgery of the lens and posterior segment of the eye to be performed. Pharmacological mydriasis can affect IOP and has been reported in horses,1 cats,2 dogs,3 and humans.4,5 Birds are unique in regard to pharmacologically induced mydriasis. In birds, topical ophthalmic administration of parasympatholytic or sympathomimetic drugs is ineffective for induction of mydriasis owing to the presence of uveal striated muscle fibers.6–8 For raptors specifically, mydriasis can be achieved by general anesthesia9,10 or the local use of neuromuscular blocking agents, which can be administered intracamerally7 or topically in conscious birds.11 A protocol involving topical ophthalmic instillation of rocuronium bromide has proven to be safe and effective for mydriasis in raptors.12–14
To our knowledge, data regarding the effect of pharmacologically induced mydriasis on the IOP of raptors are lacking. The aim of the study reported here was to evaluate the effect of rocuronium bromide–induced mydriasis on the IOP of common kestrels (Falco tinnunculus) and little owls (Athene noctuae). We hypothesized that topical ophthalmic instillation of rocuronium bromide to induce mydriasis would produce only a mild increase in or have no effect on the IOP of those 2 species.
Materials and Methods
Animals
The study reported here was conducted in strict accordance with the recommendations of the European Parliament and Council Directive 2010/63/EU and guidelines established by the Association for Research in Vision and Ophthalmology. The study protocol was reviewed and approved by the Committee of the Ethics of Animal Experiments of the University of Pisa (permit No. 37070/2013).
Thirteen common kestrels and 13 little owls were used for the study. All birds had been hospitalized at a rescue center for at least 1 month prior to study initiation and were accustomed to being handled. All birds were adults and were considered healthy with no evidence of systemic or ophthalmic disease on the basis of results of physical and ophthalmic examinations, behavior, body temperature, Hct, serum total protein concentration, and microscopic examination of a peripheral blood smear. The ophthalmic examination included a Schirmer tear test,a slit-lamp biomicroscopy,b and rebound tonometryc to measure the IOP.
Study design
The study had a within-subject experimental design such that each bird served as its own control. There were 2 treatment periods (rocuronium bromide and control) with a 1-week washout period between treatment periods. All birds were administered rocuronium bromide during the first treatment period. No ophthalmic treatments were administered during the second (control) treatment period. This study design was selected to control the possible effects of daily fluctuations and repeated measurements on the IOP.
Induction of mydriasis
A 10-mg/mL (1%) aqueous solution of rocuronium bromided was used to induce mydriasis in both eyes of each bird. The rocuronium bromide was topically administered to each eye at a dose of 0.12 mg (12 μL) for kestrels and 0.20 mg (20 μL) for little owls. Those doses were selected on the basis of results of other studies13,14 conducted to evaluate the safety and efficacy of rocuronium bromide in these 2 species. The rocuronium bromide was administered by use of a mechanical pipette.e
Mydriasis was assessed in a darkened room (ie, an environment that did not support residual PLR) with a 15-W halogen lamp used as the light source (selected intensity, 1/4; distance from the eye, approx 30 cm). The pupil diameter was measured manually with a pupil gaugef that was calibrated to the nearest 0.5 mm. Once mydriasis had been achieved and confirmed, observation of the fundus by indirect ophthalmoscopyg was performed.
Data acquisition
All IOP measurements were obtained by the same investigator (GB) with a rebound tonometerc set on the P setting, which is not specific to any species. The P setting was chosen owing to the lack of a tonometer internal calibration table specific for measurement of IOP in birds. During each IOP assessment, birds were manually restrained gently with care taken to avoid the application of any pressure on the neck, globe, or periocular region. The IOP of the left eye was always measured first. At each data acquisition time, the first 3 IOP measurements with low or no error were recorded for each eye, and then the mean for those 3 measurements was calculated and used for analysis purposes. Each measurement represented the mean for 6 valid bounces against the cornea as automatically calculated by the rebound tonometer.
All IOP measurements were obtained between 8 am and 5 pm during both treatment periods. Intraocular pressure was measured at baseline (ie, immediately before rocuronium bromide administration or at the beginning of the control period; T0); at 30 (T1), 60 (T2), and 120 (T3) minutes after baseline; and when the PLR returned to normal (T4). For the rocuronium bromide treatment period, the IOP was measured every 20 minutes after T3 until the PLR was completely restored, at which time the T4 IOP measurement was obtained. For the control treatment period, the T4 IOP measurement was obtained 180 minutes after T3. After the T4 IOP measurement was completed, fluorescein stain was applied to both eyes of each bird to assess the corneas for iatrogenic trauma.
The PLR was evaluated on a 3-point scale, where 0 = absent, 1 = decreased, and 2 = normal. A complete fast contraction of the iris in response to the light stimulus was considered a normal PLR.
Statistical analysis
The data distribution for all continuous variables was assessed for normality by means of the D'Agostino-Pearson test. Results were summarized as the mean ± SEM for normally distributed variables and as the median and range for non-normally distributed variables. A paired t test was used to compare the IOP for the left eye with that for the right eye of each bird at each measurement time. Results indicated that the IOP did not differ significantly between the left and right eyes of individual birds. Therefore, the mean IOP was calculated for the left and right eyes at each measurement time, and that value was used for all subsequent analyses as recommended.15 Within each treatment period and species, a 1-way ANOVA for repeated measures with a Dunnett post hoc test was used to compare the IOP at baseline (T0) with the IOP at each subsequent measurement time. A 1-way ANOVA for repeated measures with the Tukey post hoc test was used for pairwise comparisons of the mean IOP among T1, T2, T3, and T4. Within each species and measurement time, a Student t test was used to compare the mean IOP between the rocuronium bromide and control treatment periods. For all analyses, values of P < 0.05 were considered significant. All analyses were performed with commercially available software.h
Results
Birds
All birds successfully completed both treatment periods. No ocular abnormalities were observed in any bird before or during either treatment period. Fluorescein stain uptake was not observed in any bird following completion of either treatment period, which indicated that iatrogenic corneal trauma did not occur during the acquisition of serial IOP measurements.
During the rocuronium bromide treatment period, mydriasis with complete absence of the PLR was observed in all birds at T2 (60 minutes after rocuronium bromide administration). The mean ± SEM pupil diameter at T2 was 6.90 ± 0.45 mm for kestrels and 10.2 ± 0.25 mm for little owls. The median time required for the PLR to return to normal following rocuronium bromide administration was 280 minutes (range, 220 to 360 minutes) for kestrels and 340 minutes (range, 300 to 420 minutes) for little owls.
IOP
The mean ± SEM IOP over time during both treatment periods was plotted separately for kestrels and little owls (Figure 1). The mean IOP did not differ significantly from baseline at any time during the control treatment period for either the kestrels or little owls. During the rocuronium bromide treatment period, the mean IOP at baseline was 8.32 ± 0.36 mm Hg for kestrels and 8.21 ± 0.20 mm Hg for little owls. The mean IOP decreased after rocuronium bromide administration and reached its observed nadir at T2 for both kestrels (7.23 ± 0.54 mm Hg) and little owls (5.80 ± 0.40 mm Hg). In fact, the mean IOP was significantly lower than the baseline IOP for both species at all measurement times except for T1 in kestrels. Additionally, the mean IOP at T1 was significantly greater than that at T2 for kestrels, and the mean IOP at T4 for the little owls was significantly greater than the corresponding mean IOPs at T1, T2, and T3.
Mean ± SEM IOP over time for 13 healthy adult common kestrels (Falco tinnunculus; A) and 13 healthy adult little owls (Athene noctuae; B) when rocuronium bromide was (solid line) or was not (control; dashed line) administered to induce mydriasis. The study had 2 treatment periods separated by a 1-week washout period, and each bird served as its own control. During the first treatment period, a 1% rocuronium bromide aqueous solution was topically instilled in each eye at a dose of 0.12 mg (12 μL) for kestrels and 0.20 mg (20 μL) for little owls. No ophthalmic treatments were administered during the second (control) treatment period. For each bird during each treatment period, the IOP was measured for each eye immediately before rocuronium bromide administration or at the beginning of the control period (T0; baseline); at 30 (T1), 60 (T2), and 120 (T3) minutes after baseline; and when the PLR returned to normal (T4). For the rocuronium bromide treatment period, the IOP was measured every 20 minutes after T3 until the PLR was restored to normal, at which time the T4 IOP measurement was obtained. For the control treatment period, the T4 IOP measurement was obtained 180 minutes after T3. All IOP measurements were obtained between 8 am and 5 pm. For each bird at each measurement time, the mean IOP was calculated for the left and right eyes and used for analysis purposes. *Within a treatment period, value differs significantly (P < 0.05) from the corresponding baseline value. †Within a time, value differs significantly (P < 0.05) from the corresponding value for the rocuronium bromide treatment period. ‡Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T2. *Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T4.
Citation: Journal of the American Veterinary Medical Association 255, 12; 10.2460/javma.255.12.1359
Mean ± SEM IOP over time for 13 healthy adult common kestrels (Falco tinnunculus; A) and 13 healthy adult little owls (Athene noctuae; B) when rocuronium bromide was (solid line) or was not (control; dashed line) administered to induce mydriasis. The study had 2 treatment periods separated by a 1-week washout period, and each bird served as its own control. During the first treatment period, a 1% rocuronium bromide aqueous solution was topically instilled in each eye at a dose of 0.12 mg (12 μL) for kestrels and 0.20 mg (20 μL) for little owls. No ophthalmic treatments were administered during the second (control) treatment period. For each bird during each treatment period, the IOP was measured for each eye immediately before rocuronium bromide administration or at the beginning of the control period (T0; baseline); at 30 (T1), 60 (T2), and 120 (T3) minutes after baseline; and when the PLR returned to normal (T4). For the rocuronium bromide treatment period, the IOP was measured every 20 minutes after T3 until the PLR was restored to normal, at which time the T4 IOP measurement was obtained. For the control treatment period, the T4 IOP measurement was obtained 180 minutes after T3. All IOP measurements were obtained between 8 am and 5 pm. For each bird at each measurement time, the mean IOP was calculated for the left and right eyes and used for analysis purposes. *Within a treatment period, value differs significantly (P < 0.05) from the corresponding baseline value. †Within a time, value differs significantly (P < 0.05) from the corresponding value for the rocuronium bromide treatment period. ‡Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T2. *Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T4.
Citation: Journal of the American Veterinary Medical Association 255, 12; 10.2460/javma.255.12.1359
Mean ± SEM IOP over time for 13 healthy adult common kestrels (Falco tinnunculus; A) and 13 healthy adult little owls (Athene noctuae; B) when rocuronium bromide was (solid line) or was not (control; dashed line) administered to induce mydriasis. The study had 2 treatment periods separated by a 1-week washout period, and each bird served as its own control. During the first treatment period, a 1% rocuronium bromide aqueous solution was topically instilled in each eye at a dose of 0.12 mg (12 μL) for kestrels and 0.20 mg (20 μL) for little owls. No ophthalmic treatments were administered during the second (control) treatment period. For each bird during each treatment period, the IOP was measured for each eye immediately before rocuronium bromide administration or at the beginning of the control period (T0; baseline); at 30 (T1), 60 (T2), and 120 (T3) minutes after baseline; and when the PLR returned to normal (T4). For the rocuronium bromide treatment period, the IOP was measured every 20 minutes after T3 until the PLR was restored to normal, at which time the T4 IOP measurement was obtained. For the control treatment period, the T4 IOP measurement was obtained 180 minutes after T3. All IOP measurements were obtained between 8 am and 5 pm. For each bird at each measurement time, the mean IOP was calculated for the left and right eyes and used for analysis purposes. *Within a treatment period, value differs significantly (P < 0.05) from the corresponding baseline value. †Within a time, value differs significantly (P < 0.05) from the corresponding value for the rocuronium bromide treatment period. ‡Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T2. *Within the rocuronium bromide treatment period, value differs significantly (P < 0.05) from the value at T4.
Citation: Journal of the American Veterinary Medical Association 255, 12; 10.2460/javma.255.12.1359
The mean baseline IOP did not differ between the rocuronium bromide and control treatment periods for either species. The mean IOP for the control treatment period was significantly greater than the corresponding mean IOP for the rocuronium bromide treatment period at T2, T3, and T4 for kestrels and at T1, T2, T3, and T4 for little owls.
Discussion
Results of the present study indicated that topical instillation of rocuronium bromide to the eyes of common kestrels and little owls caused mydriasis as well as a significant decrease in IOP. The magnitude of the decrease in IOP was greater for little owls than for kestrels. The IOP was not compared between the kestrels and little owls of the present study because the dose of rocuronium bromide differed between the 2 species (ie, 0.12 mg/eye for kestrels and 0.20 mg/eye for little owls). The doses of rocuronium bromide administered to the kestrels and little owls of the present study were selected because they were proven to be sufficient to induce consistent mydriasis without local or systemic adverse effects in these species.13,14
Rebound tonometry was used instead of applanation tonometry to measure the IOP in the birds of the present study because it is considered reliable for measurement of IOP in raptors and does not require topical anesthesia.16–18 Additionally, rebound tonometry is well tolerated and provides rapid measurement of IOP with minimal stress in raptors,16 which is beneficial when serial measurements need to be obtained within a fairly short period of time. In the present study, all IOP measurements were obtained by use of the P setting on the rebound tonometer. We chose to use the P setting primarily because of the absence of a specific tonometer internal calibration table for measurement of IOP in birds. Additionally, only minimal differences were observed between IOP measurements obtained by applanation tonometry and those obtained by rebound tonometry with the P setting in several raptor species in a clinical setting.19 In anotherstudy,20 the accuracy and reproducibility of IOP measurements obtained by rebound tonometry with the D setting (ie, the setting for dogs and cats) were determined with IOP measurements obtained by use of a manometric device used as the referent for multiple raptor species. Results of that study20 indicate that, for raptors, there are several speciesspecific differences between IOP measurements obtained by rebound tonometry with the D setting and those obtained with a manometric device. This led to the establishment of reference intervals for IOP measurements obtained by rebound tonometry with the D setting for 10 species of raptors.18
At the present time, there is no clear consensus whether the D or P setting provides the most accurate reading when rebound tonometry is used to measure the IOP in raptors. Manometry is the gold standard for measurement of IOP. Therefore, IOP measurements obtained by use of both the D and P settings of a rebound tonometer should be compared with those obtained by manometry in a large population of raptors of various species to definitively determine which rebound tonometry setting provides the most accurate measure of IOP. In a population of screech owls (Megascops asio) in which the IOP was measured by rebound tonometry with both the P and D settings, the P setting measurement was generally lower than the D setting measurement.17 In regard to the present study, although the IOP measurements might have differed had we used the D setting instead of the P setting, it is likely that difference would have been systematic, and given that all IOP measurements were obtained with the P setting, we do not believe that the study conclusions would have differed had the D setting been used.
In cats, dogs, and humans, some drugs used to induce mydriasis also cause an increase in IOP. In ophthalmologically normal cats, the IOP was significantly greater in eyes that were topically treated with 0.5% tropicamide, 1% atropine, and 1% cyclopentolate, compared with the IOP in vehicle-treated (phenylephrine) control eyes.2 In another study21 involving ophthalmologically normal cats, topical administration of 0.5% tropicamide in 1 eye resulted in a significant increase in IOP in that eye as well as the contralateral eye, likely owing to systemic effects of the drug.21 In dogs, breed appears to be significantly associated with an increase in IOP following pharmacologically induced mydriasis, with Siberian Husky being the breed most predisposed to the development of ocular hypertension during mydriasis.3 Topical ophthalmic instillation of 1% atropine sulfate, 0.5% tropicamide, and 10% phenylephrine hydrochloride is also associated with a significant increase in IOP in ophthalmologically normal dogs of various breeds.22,23 In humans, topical ophthalmic application of 1% tropicamide and 2.5% phenylephrine causes a significant increase in IOP that lasts for approximately 4 hours.5 Hypothesized causes for the increase in IOP observed following topical instillation of mydriatics in the eyes of cats, dogs, and humans include partial mechanical obstruction of the iridocorneal angle or resistance to aqueous humor outflow owing to the collapse of the trabecular meshwork. Changes in IOP are not observed following topical application of various parasympatholytics or sympathomimetics in the eyes of sheep.24 In ophthalmologically normal horses, topical ophthalmic administration of 1% atropine had no effect on the IOP in one study,25 but was associated with a significant decrease in IOP in another study.1 The investigators of the latter study1 postulated that atropine improves uveoscleral drainage and that nonconventional mechanisms are probably responsible for increased aqueous humor outflow in equids.
Raptors have striated muscle fibers in the iris6,26; therefore, autonomic mydriatics are ineffective, and pharmocologically induced mydriasis in those species can be achieved only by administration of neuromuscular blocking agents. Induction of mydriasis in raptors by intracameral injection of d-tubocurarine has been described.7 In anotherstudy,11 the mydriatic efficacy of 3 topically applied neuromuscular blocking agents (pancuronium bromide, alcuronium chloride, and vecuronium bromide) was investigated in common kestrels. Pancuronium bromide failed to induce sufficient mydriasis for a fundic examination.11 Alcuronium chloride induced complete mydriasis, but most birds also developed local and systemic adverse effects.11 Vecuronium bromide provided effective mydriasis without adverse effects but only after 3 repeated instillations of the drug at 15-minute intervals.11 Rocuronium bromide safely and effectively induces mydriasis in raptors after a single topical instillation, and specific doses of the drug have been established for various raptor species.12–14 Rocuronium bromide is also a safe and effective mydriatic for Hispaniolan Amazon parrots (Amazona ventralis).27,28 Although rocuronium bromide is generally considered a safe and effective mydriatic in birds, the present study was the first to evaluate its effects on IOP. Results of the present study indicated that topical ophthalmic instillation of rocuronium bromide caused a significant decrease in IOP in common kestrels and little owls. However, the underlying mechanism for that decrease in IOP was not investigated and remains speculative.
In birds, the iridocorneal angle is characterized by various unique anatomic features. The angular aqueous sinus through which the aqueous humor flows from the anterior chamber is located in the scleral furrow on the internal aspect of the limbus. This sinus is divided by a septum and is wider than analogous structures present in domestic mammals and humans.29 The angular aqueous sinus is also connected with extracellular spaces so that most of the aqueous humor passes directly from its lumen to the venous intrascleral plexus, for ming the major pathway of aqueous humor outflow.30,31 An additional flow pathway has been hypothesized through the episcleral and subconjunctival veins.29,31 Despite these anatomic features, the fundamental aqueous humor outflow mechanism and flow rate appear to be similar between birds and mammals.31
It is possible that, in birds, the position and width of the angular aqueous sinus and the presence of a septum and its associated artery ensure the stability of the iridocorneal angle. That stability may minimize collapse of the iridocorneal angle during pharmacologically induced mydriasis and thereby prevent an increase in IOP. However, the decrease in IOP observed during mydriasis for the birds of the present study is more difficult to explain. Rocuronium bromide may increase aqueous humor outflow by the conventional pathway or enhance a nonconventional uveoscleral drainage mechanism as has been hypothesized for horses following topical ophthalmic instillation of 1% atropine.1 Alternatively, the decrease in IOP observed for the birds of the present study might have been caused by a partial loss of acuracy in the rebound tonometry readings. In birds, the ciliary muscle is striated and composed of 3 muscle fiber groups (anterior, internal, and posterior). The anterior fiber group, also called the Crampton muscle, extends from the sclera to the inner lamellae of the peripheral cornea. When the Crampton muscle contracts, the peripheral cornea flattens while the central portion of the cornea (central cornea) bends, which increases the refractive power during accommodation.32 It is possible that rocuronium-induced relaxation of the striated muscle fibers of the Crampton muscle may modify corneal variables, such as corneal rigidity and curvature, so that the rebound tonometer is not able to accurately measure the IOP. In human ophthalmology, it is generally accepted that rebound tonometry is dependent on corneal variables, and the thickness of the central cornea is associated with IOP.33,34 However, investigators of multiple studies34–36 have failed to identify a correlation between IOP measurements obtained by rebound tonometry and corneal curvature. Conversely, corneal rigidity is positively correlated with IOP measurements obtained by rebound tonometry.37
In the present study, topical ophthalmic instillation of rocuronium bromide resulted in a significant decrease in the IOP in ophthalmologically normal common kestrels and little owls. It also achieved transient mydriasis with complete loss of the PLR. No local or systemic adverse effects were observed in any of the birds of the present study. Thus, rocuronium bromide appeared to be a safe and effective mydriatic that did not increase the IOP in common kestrels and little owls.
Acknowledgments
The study was performed at the Department of Veterinary Sciences, University of Pisa, San Piero a Grado, Italy.
Supported in part by the Italian Ministry of Education, University and Research (MIUR), within the framework of the Italian National Grant for Fundamental Research (FFABR 2017).
The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| IOp | Intraocular pressure |
| PLR | Pupillary light reflex |
Footnotes
Dina strip Schirmer Plus, GECIS Sarl, Neung-sur-Beuvron, France.
Kowa SL-14, Kowa Co, Tokyo, Japan.
Tonovet, Icare, Helsinki, Finland.
Esmeron, Organon Italia SPA, Rome, Italy.
Pipetman (0-999 mcL), Gilson International-France SAS, Villiers-le-Bel, France.
Duchek pupil gauge, US Neurologicals LLC, Washington, DC.
Omega 180, Heine, Berlin, Germany.
Prism, version 6.0, Graphpad Software Inc, San Diego, Calif.
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