Bilateral phacoemulsification and intraocular lens implantation in a young African lion (Panthera leo)

Abstract

An 18-month-old intact female lioness (Panthera leo) was referred to the Clinica Veterinaria Roma Sud for evaluation of bilateral cataracts. Phacoemulsification and implantation of +30 diopter intraocular lens (IOL) were performed bilaterally. Seven years after surgery, the IOL remained centrally positioned and the patient had normal activity.

Cataract is defined as any opacity of the lens or its capsule (1). In young animals, cataract formation may result from nutritional imbalance, congenital malformation, trauma, genetic factors, or as a sequel to other ocular diseases such as uveitis or retinal degeneration. Congenital cataracts have been described in Persian, Birman, and Himalayan kittens, and a 3-month-old clouded leopard (2–4). In 1 study, milk replacement was the cause of cataracts, suggesting that the milk replacer used may have contained inadequate levels of arginine (5). Low levels of dietary histidine have also been implicated in the pathogenesis of cataract formation in kittens (6). Primary and inherited cataracts are rare in domestic cats. Most feline cataracts are secondary and are commonly due to uveitis (2–4).

Cataracts are common in zoo animals (7–13). An inherited basis was proposed in a 3-month-old clouded leopard with bilateral cataract, as nutritional etiology was unlikely (2). In 2003, one lioness was diagnosed with cataracts; hence all lions from the same group intended for the breeding program underwent complete ophthalmic examinations. A diagnosis of cataracts was made in 5 of these lions. Subsequently in 2010, candidate genes were evaluated for their potential role in cataract formation in these Angolan lions. The study concluded that the 14 candidate genes investigated were not involved in the cataracts observed (14). Encephalitozoon cuniculi has been described as a causative agent of cataract and uveitis in cats (15) and has also been identified as a cause of cataract in a snow leopard (11).

Phacoemulsification with intraocular lens implantation is routine surgical treatment for cataracts in dogs and cats. A few reports have described treatment of cataracts in exotic animals including a clouded leopard (Neofelis nebulosa) without intraocular lens implantation (2,7,8,12,13). The objective of the report herein was to describe, for the first time, bilateral phacoemulsification with intraocular implantation of lenses specifically manufactured for an African lion in order to achieve emmetropia.

Case description

An 18-month-old, 96-kg intact female lioness (Panthera leo) was referred to the Clinica Veterinaria Roma Sud with a history of aggressive behavior since birth and visual dysfunction.

The lioness came from a circus in France. She was weaned from her mother at the age of 5 mo. Her diet had been based on chicken, rabbit, and beef supplemented with taurine 5 mg twice a week.

The general examination performed by the referral veterinarian revealed bilateral cataracts. Results of hematology, biochemistry, and electrolyte analyses were within normal limits (16). Serological tests for feline leukemia virus (FeLV), feline immune deficiency virus (FIV), and feline coronavirus (FCoV) were negative.

Ten days after initial presentation, the lioness was sedated intramuscularly using a blowpipe with medetomidine (Domitor; Elanco, Eli Lilly, FI, Italia), 30 μg/kg body weight (BW), ketamine (Ketavet 100; Intervet Production, Aprilia, LT, Italy), 2 mg/kg BW, and butorphanol (Dolorex; MSD-Animal Health Italia, Segrate, MI, Italy), 0.1 mg/kg BW. Examination by a Board-certified ophthalmologist included slit-lamp biomicroscopy, applanation tonometry (TonoPen Vet; Mentor, Norwell, Massachusetts, USA) and indirect ophthalmoscopy (Omega 2000; Heine, Herrsching, Germany). Bilaterally dazzle reflex was present; direct, and consensual pupillary light reflexes were present but incomplete. Slit-lamp biomicroscopy showed a late-immature cataract in the right eye and an early-immature cataract in the left eye (Figures 1a, b). Mild lens induced uveitis was present in the right eye, evidenced by a slight miosis. No signs of uveitis were present in the left eye. Intraocular pressure (IOP) readings after instillation of oxybuprocaine chloride 0.4% (Novesina; Novertis, Origgio, VA, Italy) were 20 mmHg OD and 25 mmHg OS. The IOP in both eyes was within normal limits (normal range: 23.9 +/− 4.1 mmHg) (17). A bilateral examination of the posterior segment was performed 10 min after topical application of tropicamide 1% (Visumidriatic; Visufarma S.p.A. RM, Italy). The examination, although limited, was unremarkable but showed mild resistance to complete dilatation of the right eye.

Figure 1.

On ophthalmic examination, the right eye (OD) had a late-immature cataract and the left eye (OS) had an early-immature cataract present.

Physical examination was unremarkable. Phacoemulsification with intraocular lens implantation was discussed and recommended. In order to achieve emmetropic vision, the lens power was calculated using Retzlaff’s formula (Figure 2). A and B mode ultrasounds and keratometry were performed.

Figure 2.

Retzlaff theoretical formula used to calculate IOL power.

B-mode ultrasound (MyLab, Esaote Pie Medical, Italy) revealed normal posterior segments in both eyes, and lenses that were 8.6 mm thick and 22 mm in diameter. The A-mode ultrasound (BioLine; Optikon 2000, RM, Italy) showed that the axial length was 27.92 mm (+/− 1.41 mm) OD and 28.31 mm (+/− 1.02 mm) OS, and the preoperative anterior chamber depth (ACD) was 5.76 mm (+/− 1.89 mm) OD and 7.36 mm (+/− 1.41 mm) OS. Keratometry (Keratron Piccolo; Optikon 2000, RM, Italy), using the Retzlaff theoretical formula, represented by K, revealed a corneal curvature of 26.8 D +/− 1.96 SD OD and 28.48 D +/− 6.55 SD OS (Figure 3). The postoperative ACD (PACD) was calculated as the distance between the corneal epithelium and the center of the lens (equal to the preoperative ACD plus half lens thickness). Using mean axial length, K-value and estimated PACD, an IOL dioptric strength of 30.08 D for the left and 32.69 D for the right eye was calculated. An IOL with a diopter power of 30 D was manufactured for both eyes.

Figure 3.

Keratometry revealed a corneal curvature of 26.8 D +/− 1.96 SD in the OD and 28.48 D +/− 6.55 SD in the OS.

Surgical procedure

The lioness was sedated with medetomidine (Domitor; Elanco), 30 μg/kg BW, ketamine (Ketavet 100; Intervet), 2 mg/kg BW, and butorphanol (Dolorex; MSD-Animal Health), 0.1 mg/kg BW. Anesthesia was induced with propofol (Vetofol; Esteve, MI, Italy), 1 mg/kg BW, followed by endotracheal intubation, and maintained with isoflurane (IsoFlo; Esteve) and oxygen. Meloxicam (Metacam; Boehringer, S.p.A, MI, Italy), 10 mg, and ceftriazone (Rocefin; Roche, MI, Italy), 2 g, were administered systemically before surgery.

Both eyes received 4 cycles of topical dexamethasone 0.2% (Luxazone; Allergan S.p.A. RM, Italy), ofloxacin 0.3% (Exocin; Allergan) and tropicamide 0.5% with phenylephrine 20 min apart. Electroretinography (ERG) (HMsERG, RetVetCorp, Columbia, Missouri, USA) in both dim light and dark adaptation was performed before surgery. The ERG showed apparent normal A and B wave amplitudes when compared to other cats’ recordings in our database. After 20 min of dark adaptation ERG was recorded with light intensities of 10 millicandela/m² (mcd.s/m²); 3000 mcd.s/m²; 10 000 mcd.s/m². For photopic ERG study, there was a 10 min light adaptation. Electroretinography was recorded at 3 cd (32) std/cone bk 30 cd (Figure 4).

Figure 4.

Electroretinography (ERG) showed apparently normal A- and B-waves amplitudes when compared with other mammals.

The lioness was positioned in dorsal recumbency. The ocular surface was prepared with povidone iodine solution, diluted with saline 1:50, and the eyelids were prepared with a dilution of 1:10 of the same povidine iodine (18). Rocuronium (Rocuronio; Fresenius Kabi, VE, Italy), 0.3 mg/kg BW, a neuromuscular blocking agent, was injected intravenously. The lioness was ventilated with a standard animal ventilator. The left eye was operated on first. As the pupil failed to dilate fully, the cornea was irrigated with 1.0 mL of diluted epinephrine 1:10 000 (A.I.C; Teva Italia, MI, Italy). Mydriasis improved allowing us to perform the surgery. A 2-step corneal incision using a microsurgical blade n.64 (Swann-Morton, Sheffield, UK) and a keratome with a blade width of 2.8 mm (Surgical Specialties Corporation, Tijuana, Mexico) was made 1 mm from the limbal margin at the 1 o’clock position. A second incision of 1.0 mm width was made at the 10 o’clock position as a side-port incision. The anterior chamber was filled with hyaluronic acid (Viscoelastic 1.8% I-MED Animal Health, Dollard-des-Ormeaux, Quebec). A 9-mm anterior capsulotomy was made with a 25-gauge 1-inch needle and Vannas scissors. A continuous tear curvilinear capsulorrhexis (CCC) was carried out using Utrata forceps.

Phacoemulsification of the nucleus was conducted with a 30° phacoemulsification needle (Pulsar; Optikon 2000, RM, Italy). Total phacoemulsification time was 4 min and 42 s. The ultrasonic power used was 80%. The remaining cortical debris was aspirated with a 0.5-mm irrigation/aspiration (I/A) tip. The posterior capsule was vacuum-polished. An enlargement of the corneal incision up to 5 mm was made in order to introduce the lens into the capsular bag. A +30.0 diopter acrylic foldable lens with a 22-mm diameter haptic was placed (S&V Technologies; AG Acrivet, Hennigsdorf, Germany). The viscoelastic was removed by irrigation/aspiration. The wound was closed routinely with a 9-0 Polyglactin 910 suture in a simple interrupted pattern (Vicryl; Ethicon, Johnson & Johnson, St. Stevens-Woluwe, BXL, Belgium). A subconjunctival injection of triamcinolone (Kenacort; Bristol-Myers Squibb S.r.l, Italy), 20 mg, was performed. At that point, the lion became unstable and for safety reasons the surgery of the second eye was postponed. The recovery was uneventful.

After the surgery, the left eye was treated with topical antibiotic ofloxacin 0.3% (Exocin; Allergan RM, Italy) 4 times daily for 15 d. Systemic antibiotic, ceftriazone (Rocefin; Roche), 2 g, q24h, for 14 d and meloxicam (Metacam; Boehringer), 0.1 mg/kg BW, q24h for 5 d were given. The patient was moved to a 2 m² cage to apply topical medication, which was prepared in a 1-mL syringe. The needle of the syringe was manually broken off and the content was sprayed into the eye.

One week after surgery, the lioness was sedated and anesthetized following the same protocol as previously described for performing the surgery on the right eye. The left eye showed an extrusion of one of the haptics. Under general anesthesia, both eyes were prepared following the same protocol. The corneal wound incision of the left eye was opened and the anterior chamber was filled with hyaluronic acid (Viscoelastic 1.8%, I-MED Animal Health). After the haptic was trimmed, the lens was consecutively reinserted into the capsular bag. The corneal incision was sutured as previously described.

A conventional one-handed phacoemulsification was performed on the right eye. The rest of the procedure was similar to that described for the previously operated left eye. Time for the phacoemulsification was 2 min and 52 s. In order to avoid the complication encountered with the left eye, shortening of the haptics (about 1 mm each side) was performed before the insertion.

This eye received 20 mg of triamcinolone as a subconjunctival injection. The anesthesia and recovery were uneventful. The postoperative treatment was the same as described for the right eye.

One week later, the lioness was sedated with the previously described drugs. A complete ophthalmic examination was performed including slit-lamp biomicroscopy, tonometry, indirect ophthalmoscopy, and fluorescein staining. The only abnormal finding was moderate intraocular inflammation, presenting as a grade 2 aqueous flare. Triamcinolone injection (20 mg) was repeated in both eyes.

Eight weeks after the second surgery, the patient was sedated as previously described. Both eyes appeared quiet with no active intraocular inflammation clinically detectable (Figures 5a, b). Without dilatation, retinoscopy (Heine Beta 200 Ophthalmoscope; Heine Ophthalmic Instruments, Herrsching, Germany) performed at this time revealed both eyes to be within 1.5 D of emmetropia.

Figure 5.

Left and right eyes, respectively, at 8 and 9 wk after surgery, showed a well-centered intraocular lens with no signs of anterior uveitis. Emmetropic vision within 1.5 D.

The last complete ophthalmological evaluation was done 7 y after surgery. No signs of ocular discomfort or active intraocular inflammation were seen. The lioness showed quiet, normotensive eyes with good vision (Figures 6a, b).

Figure 6.

Left and right eyes, respectively, 7-year post-surgery follow-up.

Discussion

There are several reports of surgical removal of cataracts in exotic species (2,7,8,10,13). Intracapsular lens extraction has been performed previously in an African lion with anterior lens luxation (19). This case report presents a successful phacoemulsification with intraocular lens implantation in an African lion. Systemic, metabolic, or infectious diseases were not detected by hematology or serology, and clinical signs were not consistent with a systemic cause. Encephalitozoon cuniculi infection cannot be ruled out, as a test for its presence was not performed.

The patient came from a circus in France, but further information about the parents’ origin was not available. With the frequent movement of animals in a circus environment, a relationship with a group of Angolan lions in Germany cannot be totally excluded. Congenital cataracts have been described in Persian, Birman, and Himalayan kittens (3). Taking into consideration that the lioness had exhibited aggressive behavior since birth, a congenital etiology would be most likely. Surgical removal associated with post-operative medical therapy is the gold standard treatment of cataracts. If surgery is not performed, the patient must be monitored and if necessary treated medically for complications such as lens-induced uveitis (LIU), secondary glaucoma, retinal detachment, and lens luxation (3). Surgical intervention of cataracts in exotic animals may be required if limited vision becomes an obstacle to normal function (12). Phacoemulsification with intraocular lens implantation was appropriate in this case.

A diopter lens power measurement was performed in order to achieve the most correct IOL for emmetropic vision. The proper lens power was determined to be +30.0 diopters, as derived from the Retzlaff equation. At the time of the second surgery, the left eye showed an extrusion from the capsular bag of one of the haptics. The intraocular lens was too big for the capsular bag, and 1 haptic was then trimmed and reinserted into the capsular bag. The amplitude and intensity of ERG were considered to be adequate for surgical intervention, compared to those from domestic cats in our database. In small animal practice, all the patients that undergo a planned cataract surgery usually receive pre-surgical treatment. The goals are to reduce intraocular inflammation using topical anti-inflammatories and to minimize ocular microbial flora with broad-spectrum bactericidal topical antibiotics, started at least 12 to 24 h before surgery, and longer if LIU is present (3,20,21). Due to the extremely aggressive behavior of the patient, topical therapy before surgery could not be considered; therefore, it was reduced to just 4 cycles of treatment before surgery.

Bilateral phacoemulsification in dogs and cats is usually performed in a single surgery, as this has the advantage of restoring sight in both eyes with a single anesthetic episode as well as reducing the convalescent period, lowering overall cost when compared with 2 unilateral surgeries, and providing a higher percentage of patients which can regain vision from 1 or both eyes (22). In our case, due to the unstable anesthesia, we postponed the surgery in the second eye.

Small animal patients that undergo phacoemulsification receive intensive post-operative treatment with topical and systemic antibiotic and anti-inflammatory drugs, Elizabethan collar, and IOP measurements every 2 h for the first 12 h. In the present case, the treatment was reduced to topical application of ofloxacin 0.3% 4 times a day for 14 d. As sedation was required for examination, 2 postoperative evaluations were performed at 2 and 8 wk after the second surgery.

Complications following cataract surgery include corneal endothelial decompensation, uveitis, hyphema, fibrin formation, glaucoma, and retinal detachment. Moderate uveitis was observed in our patient during the first 2 wk post-surgery, gradually resolving over 8 wk. Transitory ocular hypertension occurs in 22.9% to 50% of canine cases within 72 h following cataract surgery (3,23–25).

A study on African lions (Pantera leo) compared the effect on IOP using 2 different protocols for sedation. The use of IM xylazine (1 mg/kg BW), atropine (0.02 mg/kg BW), and ketamine (10 mg/kg BW) or IM ketamine (20 mg/kg BW) followed by IV ketamine (5 mg/kg BW) and diazepam (0.5 mg/kg BW), showed an insignificant effect on IOP (26).

To the authors’ knowledge, there are no studies in veterinary medicine documenting the effects on IOP using a medetomidine, ketamine, and butorphanol combination via the IM route. A low IOP value secondary to the sedation cannot be completely ruled out.

In the last examination, all ophthalmic findings were within normal limits, and the patient showed correct visual behavior and clinical appearance. Good vision was achieved after surgery, as retinoscopy revealed both eyes being within 1.5 D of emmetropia and there was a dramatic improvement in the lioness behavior.

The data presented in this case report support the premise that +30 D IOL was an appropriate choice following lens extraction in this African lion. The haptics of the lens needed to be shortened, as the IOL was too long for this patient. Manual error during the measurement of the lens dimensions by ocular ultrasound was the most likely reason. Fortunately, shortening of the haptic was sufficient to provide excellent centration of the IOL.

To the authors’ knowledge, this is first case report of a bilateral phacoemulsification followed by intraocular lens implantation using a +30 D IOL in an African lion. A good clinical outcome is reported up to 7 y post-surgery.