Introduction

A 7-month-old (post pouch emergence) 6.25-kg sexually intact female Bennett’s wallaby (Macropus rufogriseus) was evaluated because of a 3-month history of bilateral ocular opacity. The owner had a group of 10 Bennett’s wallabies in an outdoor enclosure. The animal was hand reared by the owner after the death of its dam. At that time, the wallaby weighed 550 g and had opened eyes and fine fur and its first incisors were visible through the gingiva. These physical characteristics enabled age estimation of 170 days after reaching the pouch.¹ The wallaby was placed in a bag with hot water bottles to mimic the dam’s pouch. A commercial canine milk replacer was used to feed the wallaby, starting at 10 mL every 3 hours. Diet diversification was started 3 months later. Bilateral eye opacification was observed by the owner 5 months after hand rearing began. The animal showed great difficulty avoiding obstacles or finding food, and the owner kept the animal inside most of the time.

On physical examination, the wallaby was in good overall condition, with a body condition score of 5/9. A neuro-ophthalmic examination was performed. Vision was first evaluated by a cotton ball test, which was negative, then by menace response assessment oculus uterque or in both eyes (OU), which was absent. Palpebral, dazzle, and pupillary light reflexes were present OU. There was no pupil size asymmetry.

A Schirmer tear test was performed, with results of 17 mm/min oculus dexter or in the right eye (OD) and 14 mm/min oculus sinister or in the left eye (OS). A fluorescein dye test did not reveal any corneal ulcer OU. A thorough ophthalmological evaluation including slit-lamp biomicroscopy (Hawk Eye; Dioptrix) and rebound tonometry (Tonovet; Icare) was performed OU. The intraocular pressure was 16 mm Hg OD and 15 mm Hg OS, which was comparable to values described in western gray kangaroos (Macropus fuliginosus).² Before and after pupil dilation by use of tropicamide eye drops (1 drop every 5 minutes for 20 minutes), slit-lamp biomicroscopy did not show any corneal or anterior chamber abnormalities but revealed bilateral hypermature intumescent cataracts that prevented examination of the fundus by indirect ophthalmoscopy.

A blood sample was obtained from the ventral coccygeal vein. Results of CBC and serum routine biochemistry were unremarkable. Given the wallaby’s history and physical and ophthalmological findings, a nutritional cataract was diagnosed. To assess retinal function by electroretinography (ERG) and perform ocular ultrasonography, anesthesia was scheduled 2 weeks later.

Mydriasis was obtained with tropicamide eye drops (1 drop every 5 minutes for 20 minutes). The wallaby was premedicated with medetomidine (0.03 mg/kg, IM) and ketamine hydrochloride (2 mg/kg, IM). Afterward, general anesthesia was induced with isoflurane via a face mask (3% isoflurane in 1 L of oxygen). Because of the wallaby’s relatively narrow mouth opening, intubation with a 3.5-mm endotracheal tube was performed under endoscopic guidance and anesthesia was maintained with 2% isoflurane delivered in oxygen. A 22-gauge catheter was set in a lateral coccygeal vein, and sterile saline (0.9% NaCl) solution was delivered throughout the procedure (7 mL/kg/h).

Standardized ERG (VisioSystem; Dioptrix) was performed to check retinal function. Electrodes were placed on each upper eyelid conjunctiva and subcutaneously at the base of both ears. A reference electrode was set subcutaneously on the dorsal neck, caudal to the occiput (Figure 1). Achromatic stimulation in photopic conditions was performed, followed by a blue stimulation in scotopic conditions and another one after 8 minutes of dark adaptation. An ERG flicker test was then conducted by stationary achromatic stimulation (30 Hz). Bilateral recordings exhibited responses but of attenuated amplitude of cone and rod photoreceptors after each stimulation. Flicker stimulation in photopic atmosphere also confirmed the presence of cone activity OU (Figure 2). At 40,000 millicandela X s/m² after achromatic stimulation in photopic atmosphere, b-wave amplitudes were 25 µV OD and 35 µV OS and implicit times were 42 milliseconds OD and 41 milliseconds OS. At 40 millicandela X s/m² after 8 minutes of dark adaptation and blue stimulation in scotopic atmosphere, b-wave amplitudes were 21 µV OD and 23 µV OS and implicit times were 54 milliseconds OD and 61 milliseconds OS. On the basis of ERG results, we concluded that the wallaby would have a good chance for functional vision following phacoemulsification in the same way that some diabetic dogs with a mature cataract may have a reduced ERG response preoperatively.³

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Photograph of the position of electrodes for electroretinography in an anesthetized 7-month-old female Bennett’s wallaby (Macropus rufogriseus) with bilateral total hypermature cataracts. The electrodes were placed on each upper eyelid conjunctiva and subcutaneously at the base of both ears, and a reference electrode was set subcutaneously on the dorsal neck, caudal to the occiput.

Citation: Journal of the American Veterinary Medical Association 260, 4; 10.2460/javma.21.03.0165

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Electroretinograms of the wallaby (left) and a healthy dog (right) in different atmospheres. Note the presence but low amplitude of the waves attributed to the major opacity of both the lens and vitreous humor, compared with normal electroretinograms of the dog.

Citation: Journal of the American Veterinary Medical Association 260, 4; 10.2460/javma.21.03.0165

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Vitreoretinal ultrasonography (Oti Scan 3000; Ophthalmic Technologies Inc) was performed OU by use of a 10-MHz ultrasound probe revealing a bilaterally thickened and opaque lens and a bilaterally heterogeneous vitreous humor, without retinal detachment (Figure 3). Neither lens displacement nor spontaneous lens capsule rupture were observed.

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Ultrasound image of the right eye of the wallaby in Figure 1, obtained with the wallaby anesthetized. A thickened and opaque lens (L) and heterogeneous vitreous humor (V) are evident, without retinal detachment.

Citation: Journal of the American Veterinary Medical Association 260, 4; 10.2460/javma.21.03.0165

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Because no contraindication was found, surgery was performed to improve animal welfare. The anesthetized wallaby was placed in lateral recumbency; the right eye was prepared aseptically with diluted 5% povidone-iodine solution and draped routinely. A stay suture was placed on the lateral bulbar conjunctiva using a 5-0 polypropylene suture material. A 3.2-mm clear corneal incision was made in 1 step by use of a 3.2-mm angled microsurgical knife (Unique Technologies; Figure 4). After the inflation of the anterior chamber with 1.6% sodium hyaluronate viscoelastic substance (Ophteis Bio 1.6; Rayner) and anterior capsulorhexis, phacoemulsification (1-handed technique) was completed with a phacoemulsification unit (Infiniti; Alcon) through the corneal incision, followed by meticulous irrigation-aspiration of the residual cortical material and polishing of the posterior capsule, without intraocular lens implantation. The anterior chamber was narrow due to the intumescent lens.

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Step-by-step photographs obtained during surgical management of the bilateral cataract in a Bennet’s wallaby (right eye shown). A—The 3.2-mm clear corneal incision. B—Injection of the viscoelastic substance in the anterior chamber. C—Phacoemulsification. D—Eye appearance after phacoemulsification; note the vitreous humor opacity. E—Vitrectomy through the initial keratotomy incision. F—Final ocular appearance before corneal suture.

Citation: Journal of the American Veterinary Medical Association 260, 4; 10.2460/javma.21.03.0165

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Following phacoemulsification, total opacification of the vitreous humor was revealed. This opacification prevented visualization of the fundus (Figure 4). After posterior capsulorhexis was performed, a deep and large anterior vitrectomy was performed to clear the ocular media. Vitrectomy was performed by a limbic anterior approach through the initial keratotomy incision and was as complete as possible. The cut rate was 600 cuts/min, and the vacuum level was 200 mm Hg.

The corneal incision was closed with 6 simple interrupted sutures of 9-0 polyglactin 910. Tissue plasminogen activator (Actilyse; Boehringer Ingelheim; 25 µg) was injected into the anterior chamber to avoid fibrin formation with a 30-gauge needle next to the incision. The animal was repositioned, and the same procedure was repeated for the left eye. Affected lenses were soft, and short phacoemulsification times were necessary for their surgical removal (95 seconds OD, and 76 seconds OS).

Intravenous dexamethasone (0.1 mg/kg) and subconjunctival methylprednisolone acetate (5 mg) were administered perioperatively. Anesthesia was reversed with atipamezole (0.16 mg/kg, IM), and the wallaby recovered uneventfully. The animal was discharged from the hospital with the following prescription: meloxicam (0.2 mg/kg, PO, q 24 h for 5 days), amoxicillin–clavulanic acid (15 mg/kg, PO, q 12 h for 7 days), and dexamethasone–neomycin sulfate–polymixin B sulfate ophthalmic solution (Maxidrol; 1 drop OU, q 12 h for 1 month). An Elizabethan collar was not considered as an option given the liveliness, locomotion, and feeding methods of wallabies.

Two days after surgery, the owner reported the wallaby had mild diarrhea, which worsened over the next 4 days. Oral antimicrobial therapy was discontinued, and the diarrhea quickly resolved.

The wallaby was reevaluated 10 days following cataract surgery. An obvious behavioral improvement was noticed by the owner. Neuro-ophthalmic examination showed that the wallaby was able to move around the consultation room without hitting any obstacles and without hesitation. The cotton ball test was negative, but a false-negative result was deemed possible considering the species and the animal’s state of stress during the examination. The menace response was present OU, as well as the dazzle, palpebral, and pupillary light reflexes. Intraocular pressure measurements were 12 mm Hg OD and 14 mm Hg OS. Mild bilateral corneal edema was present, with no signs of discomfort (Figure 5). A trace aqueous flare was also noticed OU. There was neither retinal detachment nor retinal hemorrhage.

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Appearance of the eyes at various points. A—Left eye 10 days postoperatively. B—Right eye 1 year after the surgery. C—Left eye 1 year after the surgery. Note in panels B and C that the bilateral peripheral posterior capsular opacification does not interfere with the visual axes due to the width of the posterior capsulorhexis.

Citation: Journal of the American Veterinary Medical Association 260, 4; 10.2460/javma.21.03.0165

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The owner provided monthly updates, as follows: the wallaby joined its conspecifics outdoor 1 month after surgery, was completely independent at that time, and appeared to have excellent ocular comfort. A recheck examination 1 year after initial presentation did not reveal any inflammation (Figure 5). Intraocular pressures were 15 mm Hg OD and 17 mm Hg OS. Bilateral peripheral posterior capsular opacification was present, without obstruction of the visual axes due to the large size of the posterior capsulorhexis OU. The wallaby wandered easily in the exam room, avoiding obstacles. The owner confirmed the wallaby had good daily autonomy and the ability to move and jump normally.

Discussion

Among ophthalmological disorders of macropods, cataracts are rather common.⁴ Trauma-induced cataracts as well as infectious causes are described.^4,5 In chronic cases, toxoplasmosis could provoke unilateral or bilateral cataracts in wallabies associated with gastrointestinal, respiratory, or neurologic signs.^6,7 Encysted bradyzoites and free tachyzoites of Toxoplasma gondii have been found in the eyes of affected animals. In the present case, the age of the wallaby, unremarkable physical findings except for bilateral mature cataracts, and history of hand rearing with a commercial canine milk replacement led us to rule out toxoplasmosis and diagnose nutritionally induced cataracts.

Lactation of the tammar wallaby (Macropus eugenii) has been extensively studied, and milk analyses have also been performed in Bennett’s wallabies.^8–11 Drastic changes in milk composition are described over time in these 2 species. The total solids level increases gradually. Protein and lipid levels are low and carbohydrates level high, but between 200 and 300 days of lactation, the trend reverses and the carbohydrates level falls below 2%.^9,11 The type of carbohydrates varies, as follows: mainly oligosaccharides before 300 days of lactation and almost exclusively monosaccharides (galactose and glucose) afterward.¹¹ The commercial canine milk replacer used by the owner contained 29% carbohydrates (mainly lactose), 25% proteins, and 24% fat. Therefore, the composition was not adapted to the wallaby needs and the lactose overload was likely the reason for cataract development.

Numerous theories have been proposed to explain cataracts in pouch-young macropods. Lactose is digested into galactose and glucose. In humans, blood galactose levels are kept at negligible levels by efficient use of galactose.¹² Galactose is metabolized by liver enzymes such as galactokinase and galactose-1-phosphate uridyl transferase. A primary or acquired deficiency of these hepatic enzymes is suspected to be the cause of galactosemic cataract in a range of marsupials. Indeed, very low activity level of the 2 aforementioned enzymes have been demonstrated in several species of marsupials.¹³ It was supposed that with low levels of these enzymes, macropods fed lactose-containing milk formulas would develop a galactosemia and subsequent galactosemic cataracts due to an inability to convert galactose. Although hand-reared joeys are particularly sensitive to this condition, cataracts can also develop in joeys raised naturally. Given that the disease has been observed in wild macropods and that feeding of lactose-enriched milk formulas does not automatically lead to cataract formation, other etiologies could be possible.⁴ A deficiency of a protein or particular amino acid has been proposed.¹⁴ In other species, several nutritionally induced cataracts have been reported due to amino acid deficiencies, including histidine, tryptophan, phenylalanine, and arginine.^15,16

Nutritional cataracts progress quickly in wallabies and can mature within 1 or 2 weeks. Glaucoma secondary to chronic uveitis with mature cataract occurs frequently in kangaroos. Posterior lens luxation into the vitreous humor may also occur in some cases of mature cataracts.⁵ There was no uveitis in the wallaby of the present report, and such complications were not observed.

Some ERG values have been published for tammar wallabies and western gray kangaroos.^17,18 Although the ERG stimulation settings were not the same as for these other animals, comparison with these previously published results revealed lower b-wave amplitude values in the wallaby of the present report and relatively comparable implicit times. The low amplitude of the waves could have been attributable to the major opacity of both lens and vitreous humor in the same way that some diabetic dogs with a mature cataract may have a reduced ERG reading preoperatively.³ It is worth noting that the dark adaptation time in our protocol was shorter than the typical 20 minutes to limit the duration of general anesthesia, knowing that bilateral cataract surgery was potentially to follow. Electroretinography was performed to assess retinal electrical function because opaque ocular media precludes direct examination of the posterior segment. Combined with eye ultrasonography of the eye, ERG revealed functional retinae and no contraindication to the surgery.

Even if detailed reports of surgical management of nutritional cataracts in macropods are lacking in literature, surgery is considered without any particular challenge in kangaroos.⁵ As in the present case, pupils dilate properly with tropicamide and short phacoemulsification times are necessary, likely due to soft cortical and nuclear material. Phacoemulsification has been described in a large variety of species. Specific anatomical variations could be challenging in some species, such as scleral ossicles in birds¹⁹ or spectacles in snakes,²⁰ but no difficulties were encountered in the wallaby of the present report. There was no major difference between our surgical technique and the one used in other mammals with a 1-handed technique. The extensive bilateral vitreous humor opacification encountered in the wallaby has been described in kangaroos, requiring bilateral deep and large vitrectomy.⁴ The conventional approach of posterior vitrectomy usually performed through the pars plana could not be considered in this case. We therefore decided to continue the vitrectomy via the limbic anterior approach, without a posterior segment visualization system. As the vitreous humor was very dense and whitish in appearance, it was very easily visualized, allowing control of the vitrectomy in depth in the posterior segment by varying the focal distance through adjusting the focus of the microscope and the mobile surgical table. The anterior vitrectomy was not complete, especially peripheral vitreous humor, but a total transparency of the visual axis was restored. The vitreous humor opacity could be caused by a high vitreous humor concentration of galactose, as shown by analysis of the vitreous humor in a kangaroo.⁵

Posterior capsular opacity is the most common long-term complication of phacoemulsification in dogs,²¹ cats,²² and birds,^19,23,24 occurring in 36% to 100% of patients, depending on the study. It is caused by proliferation and migration of residual lens epithelial cells. Although our wallaby developed a mild peripheral posterior capsular opacification, the animal had vision OU and its quality of life greatly improved. Vision-threatening complications such as glaucoma and retinal detachment were not observed. Phacoemulsification success rates between 78% and 95% are reported in the literature in dogs,²¹ cats,²² birds,^19,23,24 rabbits,²⁵ and loggerhead turtles (Caretta caretta).²⁶ Kangaroos are prone to developing glaucoma 2 to 12 weeks postoperatively.^4,5 This common complication of cataract surgery frequently results in globe evisceration or euthanasia in this species.⁵ The prognosis is generally poor, and cataract surgery is not recommended in the macropod literature. In the wallaby, we did not encounter intraoperative lens instability or postoperative glaucoma and the intraocular inflammation was well controlled by postoperative therapy. Long-term recovery of vision was very satisfactory; however, additional research involving more Bennett’s wallabies is needed to evaluate whether cataracts are systematically associated with vitreous humor opacification and confirm the justification for cataract surgery in this species.