Phacoemulsification of bilateral mature cataracts in a Texas rat snake (Elaphe obsoleta lindheimeri)

Eric C. Ledbetter Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Ricardo de Matos Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Rebekah M. Riedel Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Teresa L. Southard Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Abstract

CASE DESCRIPTION A 10-year-old sexually intact male client-owned Texas rat snake (Elaphe obsoleta lindheimeri) was referred for evaluation because of a 5-month history of progressive bilateral ocular opacities and abnormal behavior.

CLINICAL FINDINGS On ophthalmic examination, the snake had bilateral mature cataracts and uveal cysts. No additional ophthalmic or physical abnormalities were detected. Results of CBC, serum biochemical analysis, and ocular ultrasonography were unremarkable.

TREATMENT AND OUTCOME Bilateral spectaculotomy was performed, followed by bilateral phacoemulsification and uveal cyst aspiration, without complication. Histologic evaluation of the phacoemulsified lens material revealed only nonspecific findings associated with cataractogenesis. Vision was restored and the abnormal behaviors resolved after cataract surgery. Long-term follow-up examination performed 60 weeks after surgery revealed no additional ocular or physical abnormalities.

CLINICAL RELEVANCE The ocular anatomic and physiologic characteristics of snakes can pose intraoperative and postoperative challenges to phacoemulsification, but the outcome achieved for this surgical case suggested that successful cataract surgery is possible in these species. This case further demonstrated that cataracts may be associated with reversible behavioral abnormalities in captive snakes.

Abstract

CASE DESCRIPTION A 10-year-old sexually intact male client-owned Texas rat snake (Elaphe obsoleta lindheimeri) was referred for evaluation because of a 5-month history of progressive bilateral ocular opacities and abnormal behavior.

CLINICAL FINDINGS On ophthalmic examination, the snake had bilateral mature cataracts and uveal cysts. No additional ophthalmic or physical abnormalities were detected. Results of CBC, serum biochemical analysis, and ocular ultrasonography were unremarkable.

TREATMENT AND OUTCOME Bilateral spectaculotomy was performed, followed by bilateral phacoemulsification and uveal cyst aspiration, without complication. Histologic evaluation of the phacoemulsified lens material revealed only nonspecific findings associated with cataractogenesis. Vision was restored and the abnormal behaviors resolved after cataract surgery. Long-term follow-up examination performed 60 weeks after surgery revealed no additional ocular or physical abnormalities.

CLINICAL RELEVANCE The ocular anatomic and physiologic characteristics of snakes can pose intraoperative and postoperative challenges to phacoemulsification, but the outcome achieved for this surgical case suggested that successful cataract surgery is possible in these species. This case further demonstrated that cataracts may be associated with reversible behavioral abnormalities in captive snakes.

A 10-year-old 0.98 kg (2.2-lb) sexually intact male client-owned Texas rat snake (Elaphe obsoleta lindheimeri) was referred to the Cornell University Hospital for Animals for evaluation of presumed cataracts. Bilateral ocular opacities that had progressively increased in size and density were first noticed by the owner approximately 5 months prior to initial evaluation. A decrease in typical activity level as well as abnormal behaviors (ie, aggression toward the owner, striking randomly, and slower ability to locate offered food) were also observed during this period.

The snake had undergone normal ecdysis approximately once per month during the interval since the abnormalities were first noted. It was fed 1 frozen rat or mouse/wk and was kept in a terrarium with an under-the-tank heater system that maintained a temperature gradient from 34° to 22°C (93° to 72°F) in nonheated tank areas. Tank temperatures were routinely spot checked with an infrared thermal scanner. Aspen tank bedding was used in the terrarium and regularly replaced. A natural light cycle that was adjusted for the season was maintained by a light-emitting-diode tank light. Humidity in the tank was kept at approximately 60%. The snake had no history of other illnesses in the 6 years since it was acquired by its current owner.

On initial evaluation, physical examination findings were unremarkable and the snake was active and responsive. Ophthalmic examination by slit-lamp biomicroscopya revealed bilateral mature cataracts (Figure 1). Darkly pigmented uveal cysts were also identified in each eye (3 cysts in the right eye and 2 cysts in the left eye) that could be transilluminated with a strong focal light source. The uveal cysts originated from the posterior iridal surface, wrapped around the pupillary margin, and were associated with focal and mild dyscoria. The pupillary light reflex was intact, and the anterior chamber was clear in both eyes. Fundus examinationb was attempted but precluded by the cataracts. No additional ophthalmic abnormalities were detected.

Figure 1—
Figure 1—

Photographs of the left eye of a client-owned Texas rat snake (Elaphe obsoleta lindheimeri) before (A) and 60 weeks after (B) cataract surgery. A—A mature cataract, 2 uveal cysts, and mild dyscoria are visible. B—Aphakia with a clear spectacle, cornea, and lens capsule are present.

Citation: Journal of the American Veterinary Medical Association 251, 11; 10.2460/javma.251.11.1318

Serum biochemical and hematologic analyses were performed on a cardiocentesis sample, and all values were within reference ranges for rat snakes.1 Bilateral ocular ultrasonography was performed with a 20-MHz transducerc and a water-filled standoff pad. With the exception of the cataracts, no abnormalities were identified in either eye (Figure 2). Electroretinography was not performed because reference values for colubrid species have not been established.

Figure 2—
Figure 2—

Ultrasonographic image of the left eye of the snake in Figure 1 obtained with a 20-MHz transducer prior to cataract surgery. The cataract is associated with an increase in echogenicity of the lens, but the eye is otherwise unremarkable.

Citation: Journal of the American Veterinary Medical Association 251, 11; 10.2460/javma.251.11.1318

The following day, the snake was premedicated with meloxicam (0.5 mg/kg [0.23 mg/lb], SC), ceftazidime (20.0 mg/kg [9.1 mg/lb], IM), and butorphanol tartrate (5.0 mg/kg [2.3 mg/lb], IM). General anesthesia was induced with inhaled isoflurane delivered with a mask. Endotracheal intubation was performed, and anesthesia maintained with sevoflurane in oxygen. During anesthesia, heart rate was monitored by use of a Doppler ultrasonic flow detector positioned over the heart, and body temperature was tracked with an esophageal thermometer. Respiratory rate was monitored by observing the breathing bag in the nonrebreathing anesthesia circuit until apnea occurred. Once apnea was noted, positive pressure ventilation was initiated and maintained at a rate of 4 breaths/min.

The spectacle and periocular scales were aseptically prepared with 10% povidone-iodine solution, and the right periocular area was draped. The snake's head was positioned under an operating microscope so that the right ocular surface was parallel to the top of the operating table. A lateral approach to the eye was used to avoid the prominent supraocular scales. A stay suture of 6-0 polyglactin 910d was placed in the spectacle 2 mm posterior to the underlying lateral corneal limbus for manipulation of the spectacle during surgery. The spectacle was scored with a microsurgical scalpel bladee in an elliptical pattern following the course of the underlying corneal limbus. To allow the spectacle to be safely incised, 2% hydroxypropyl methylcellulose viscoelastic solutionf was injected with a 25-gauge needle through the spectacle score to expand the subspectacular space. An approximately 4.0-mm spectaculotomy incision was then made by cutting with Vannas scissors along the previously created spectacle score. Gentle manual traction on the spectacle stay suture caused the spectacle incision to slightly separate, allowing access to the globe. A conjunctival stay suture of 6-0 polyglactin 910d was placed 1.0 mm posterior to the limbus for stabilization of the globe during surgery.

A 2.6-mm stepped clear corneal incision was made with a microsurgical scalpel bladee followed by a 2.6-mm keratome. The aqueous humor was replaced by injecting 2% hyaluronic acid viscoelastic solutiong into the anterior chamber. Mechanical pupillary dilation with viscoelastic solution yielded approximately 50% mydriasis. Atracurium besylateh (0.1 mL of a 10 mg/mL solution diluted in balanced salt solution to 1.0 mg/mL) was administered into the anterior chamber and, after a 5-minute period, resulted in a modest additional improvement in pupillary dilation. A 27-gauge needle was used to perform an anterior capsulotomy, and a continuous curvilinear capsulorrhexis was completed with Utrata forceps.

Phacoemulsification was performed with a phacoemulsification unit,i 0.9-mm ultrasonic tipj with a 30° bevel, and enriched balanced salt irrigation solution.k During the course of the lens removal, surgery was repeatedly suspended for several minutes when the spectacle vasculature filled with flowing columns of blood, limiting intraocular visibility. Repeated topical application of 1.0% phenylephrine solutionl had no appreciable effect on the spectacle blood vessels. The small size of the anterior chamber and lens capsule necessitated sequential segmentation of the lens nucleus and segment manipulation to the far side of the lens capsule, away from the incision, for emulsification and extraction. This approach was used to avoid anterior chamber collapse resulting from aspiration while the handpiece irrigation ports were positioned outside the corneal incision. Although the lens nucleus was dense, its small size permitted rapid ultrasonic segmentation, emulsification, and aspiration. During the process of phacoemulsification, the uveal cysts detached and were aspirated without hemorrhage or other complications. An irrigation-aspiration handpiece was used to remove the copious amounts of remaining lens cortical material and to polish the anterior lens capsule. Viscoelastic solution was then evacuated from the anterior chamber and replaced with irrigation solution.

The corneal incision was closed with 2 simple interrupted sutures of 9-0 polyglactin 910.d Single drops of 0.3% ofloxacin ophthalmic solutionm and 1.0% prednisolone acetate ophthalmic solutionn were instilled into the subspectacular space, and the spectaculotomy incision was closed with 9-0 polyglactin 910d in a simple interrupted pattern. The snake was repositioned, and the same procedure was repeated for the left eye. Duration of ultrasound application was 9.6 seconds, with 11.3% power in the right eye, and 11 seconds, with 18.7% power in the left eye. Samples of the phacoemulsified lens material from both eyes were removed from the phacoemulsification drainage cassette and evaluated by histologic examination. Morgagnian globules, which appeared as swollen and rounded lens fibers, were identified in the small lens segments (Figure 3). No infectious agents or inflammatory cells were detected in the lens material.

Figure 3—
Figure 3—

Photomicrograph of a sample of phacoemulsified lens material from the snake in Figure 1. The lens contains Morgagnian globules, but no infectious agents or inflammatory cells are visible in the lens material. Scattered erythrocytes and pigment granules are also visible. H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 251, 11; 10.2460/javma.251.11.1318

The snake recovered from anesthesia without complication and remained hospitalized for 2 days after surgery. During hospitalization, 0.3% ofloxacin ophthalmic solution (1 drop in each eye, q 6 h), 1.0% prednisolone acetate ophthalmic solution (1 drop in each eye, q 6 h), and meloxicam (0.5 mg/kg, SC, q 24 h) were administered. The morning after surgery, focal corneal edema was evident around the incisions, mild aqueous flare was present in the anterior chambers, and the pupils were midrange in diameter and responsive. Examination of the fundi by indirect ophthalmoscopy yielded unremarkable results. On the second day after surgery, the aqueous flare was reduced and the other ophthalmic examination findings were unchanged. The snake was discharged from the hospital with instructions for the owner to administer 0.3% ofloxacin ophthalmic solution (1 drop/eye, q 6 h until recheck examination), 1.0% prednisolone acetate ophthalmic solution (1 drop/eye, q 6 h until recheck examination), meloxicam (0.5 mg/kg, SC, every other day for 6 days), and ceftazidime (20.0 mg/kg, IM, every third day for 6 days).

The snake was reevaluated 2 weeks following cataract surgery. The owner reported observing an immediate increase in the snake's activity level, cessation of aggressive behaviors, resolution of the random striking, a more rapid ability to locate food, and an increase in environmental exploration when the snake returned home after surgery. During ophthalmic examination, white deposits (interpreted as dried prednisolone acetate solution) were identified on the spectacle surface and adherent to the spectacle sutures, the spectacle appeared moderately opaque immediately adjacent to the incision, and the subspectacular space was mildly distended by clear fluid in both eyes. Focal peri-incisional corneal edema and vascularization were present. The anterior chambers were clear, the pupils were responsive, and the lens capsules were clear. The right pupil was mildly dyscoric. The fundus appearance was unremarkable in both eyes. All medications were discontinued.

Recheck examination was performed 5 weeks after cataract surgery. The intraocular findings were unchanged from the previous examination. The sutures in the spectacle remained, and opacification of the spectacle in the region of the incision had increased in area and was now intermixed with continuously patent spectacular blood vessels. The sutures in the cornea were no longer visible, and the corneal edema and vascularization had resolved. Treatment with an artificial tear gel solutiono was started (1 drop/eye, q 8 h until recheck examination) to maintain spectacle moisture and encourage normal shedding. Recheck examination at 14 weeks after cataract surgery revealed similar findings, with slight progression of the spectacle opacification and persistent spectacle sutures. Intraocular findings remained unchanged. Manual removal of the sutures was attempted with a cotton-tipped swab and Colibri forceps but was unsuccessful. The owner reported that the snake had not undergone ecdysis since cataract surgery and was instructed to continue administration of artificial tear gel solution until the next shedding cycle.

The next recheck examination was performed 26 weeks after cataract surgery. The owner reported the snake had had 3 ecdysis cycles since the previous evaluation; each had been associated with an incremental reduction in the area and density of the spectacular opacities. The shed exuvium from the most recent ecdysis was presented by the owner for examination, and the spectacles appeared to have shed normally and completely. The spectacle sutures were no longer present. Small (< 1.0-mm) focal opacities remained in each spectacle in the region of the previous sutures, but each spectacle was now otherwise clear and devoid of visible patent blood vessels. The intraocular findings were unchanged from the previous examination, the lens capsules remained clear, and the owner continued to report a return to usual activity level and behavior for the snake.

On recheck examination performed 60 weeks after cataract surgery, the snake continued to behave and eat normally. With the exception of the faint spectacle cloudiness and microabrasions expected for a snake in a pre-ecdysis period, the spectacle in both eyes was clear with no opacities or blood vessels visible (Figure 1). The corneas and anterior chambers appeared unremarkable with no visible incisional scars. Punctate accumulations of transparent material (presumed cortical regrowth) were visible on the posterior lens capsules, but the lens capsules remained clear. Results of fundus examination of both eyes were unremarkable.

Discussion

Successful cataract removal by phacoemulsification has not been previously reported for snakes and is uncommonly described for any reptilian species. Clinical reports of cataract surgery in reptiles include those of a loggerhead sea turtle2 (Caretta caretta), savannah monitor3 (Varanus exanthematicus), black water monitor4 (Varanus salvator macromaculatus), and Komodo dragon5 (Varanus komodeonsis). These published surgical descriptions for large reptilian species differ considerably from that for the Texas rat snake in the present report because of the smaller eye size and presence of a spectacle in snakes.

Snake ocular anatomic and physiologic characteristics also pose various surgical challenges distinct from most mammalian and avian species in which cataracts are more routinely treated by phacoemulsification.6–8 The small size of the cornea, anterior chamber, and lens in snakes are poorly suited for most available phacoemulsification unit handpieces and equipment.9–11 In snakes, embryonic eyelid fusion forms the spectacle,12 which is a layer of transparent integument covering the cornea and tear-filled subspectacular space that provides both protective and optical refractive functions.13,14 The spectacle is attached to the periocular scales, but not to the globe.15,16 Surgical instrument insertion through the spectacle and corneal incisions was often difficult with the snake of the present report because the globe moved independently of the spectacle and alignment of the incisions was not always present or readily achievable.

The surgeon's ability to see the lens of the Texas rat snake was impeded by the failure to achieve maximal mydriasis with general anesthesia alone. Parasympatholytic and sympathomimetic agents commonly used to induce mydriasis in mammals are ineffective for the striated muscles of the snake iris.17,18 Intracameral injection of a neuromuscular blocking agent during the surgery, as previously described for a turtle,2 was only partially effective in improving pupillary dilation. The spectacle vasculature was an additional obstacle to the surgeon's ability to see the lens.19 The repeated filling of the spectacle blood vessels was an unexpected occurrence and did not appear associated with any specific surgical manipulations. When snakes are at rest, spectacle blood vessels undergo cycles of dilation and constriction, with the vessels spending most of the cycle maximally constricted to remove them from the visual field.20 When snakes are distressed or encounter a visual threat, spectacle vessels remain constricted for longer periods than during the normal resting cycle to optimize vision. During the renewal phase of the snake integument, the resting cycle is abolished and the spectacle vessels remain dilated, which is presumed to support cellular proliferation and generation of a new stratum corneum.20 It is likely that general anesthesia, surgical manipulation, or changes in ambient temperature temporarily disrupted the normal blood flow dynamics of the spectacles in the snake of the present report.

In addition to providing intraoperative challenges during cataract surgery, the spectacle complicates pre-and postoperative medication administration to snakes. No detailed studies have been performed to characterize the specific barrier properties of the spectacle; however, the spectacle is commonly believed on the basis of anatomic considerations to be impermeable and to render topical ophthalmic medications ineffective.12 For this reason, the snake of the present report was given antimicrobials and anti-inflammatories parenterally before and after cataract surgery. In addition, topical ophthalmic medications were administered in the immediate postoperative period because we surmised that the spectacle incision or sutures might temporarily compromise the impervious barrier of the spectacle and permit penetration to the globe. An alternative approach that we considered was to leave the spectacle incision unsutured and open to permit topical medication delivery after surgery. Leaving the spectacle defect open might have increased the risk of exposure keratitis and might not have succeeded in allowing access of topically applied medications to the eye, given that a proteinaceous plug of material forms rapidly in spectacle wounds that may limit or block medication penetration.21

The postoperative changes clinically observed around the spectaculotomy sites in the snake of the present report were similar to those reported for a clinical and histologic study,21 in which the course of spectacle wound healing was examined following partial spectaculectomy in ball pythons (Python regius). In that study, edema, vascularization, and opacification of the spectacle were observed in the first weeks after removal of a wedge of spectacle. By 3 months after spectaculectomy, normal spectacle morphology and transparency were achieved clinically and histologically.21

The cause of the cataracts and uveal cysts in the snake of the present report was not identified. Cataracts in reptilian species are infrequently reported, but general categories of cataract etiologies in other species include genetic abnormalities, uveitis, metabolic systemic diseases, lens trauma, nutritional deficiencies, sequelae to other structural ocular abnormalities, radiation exposure, and toxicants.22–24 Histologic evaluation of the removed snake lens fragments revealed Morgagnian globules, which are a common and nonspecific histologic change associated with cataract formation, but did not provide any etiologic information.25,26 Uveal cysts have been identified in various animal species and originate from the posterior pigmented iris epithelium or the ciliary body epithelium.27 The cysts may be congenital or acquired in origin, with trauma and uveitis as proposed etiologies of acquired cysts.28 The uveal cysts in the snake of the present report may have formed secondary to lens-induced uveitis; however, no clinical evidence of active uveitis was appreciated during ophthalmic examination prior to phacoemulsification. Although the impact of the uveal cysts on ocular health and vision appeared minimal relative to the cataracts, large uveal cysts in other species may be associated with impaired vision, damage to the corneal endothelium, marked distortion of the iris, and secondary glaucoma.29–31

Vision plays a key role in defensive strike targeting and detection, location, and capture of prey for many snake species.32,33 In addition to vision, many snake species use olfaction or infrared radiation detection to locate prey, predators, and shelter.34–37 As a result, impaired vision may not preclude normal feeding behavior in many snakes, particularly when dead prey are fed to captive snakes, and not all snakes with cataracts will require surgery to preserve general health.38 Diurnal colubrid species such as rat snakes have highly evolved visual systems for their ecological niche that typically include cone-rich retinas and a high ratio of optic nerve fibers to photoreceptors.39,40 Visual acuity measurements in midland water snakes (Nerodia sipedon pleuralis), which are colubrids related to rat snakes, reveal a spatial resolution similar to that of domestic cats.41 Snake visual systems evolved to permit a wide range of environmental interactions, not just feeding, which has historically been the focus of most snake vision research.42–44 Although vision deprivation associated with the cataracts did not prevent the snake of the present report from feeding, development of abnormal behaviors and a reduced activity level coincidental with cataract formation prompted surgical removal of the cataracts. These abnormalities resolved after surgery.

Altered behavior resulting from cataract-induced vision loss is not an unexpected situation for snakes given that abnormal behavior (eg, signs of irritability, lethargy, and aggression) attributed to impaired vision is common in some snakes in association with spectacle opacification during ecdysis or dysecdysis.45,46 Although the ocular anatomic and physiologic characteristics of snakes can pose challenges to successful phacoemulsification, the outcome for the snake of the present report suggested that modern cataract surgery is possible in these species and that cataracts may be associated with reversible abnormal behavior in captive snakes.

Acknowledgments

The authors thank Jonah Marion for providing technical and historical information.

Footnotes

a.

Kowa SL-15 portable slit-lamp, Kowa Co, Tokyo, Japan.

b.

Heine Omega 500 binocular indirect ophthalmoscope, Dover, NH.

c.

Innovative Imaging Inc, Sacramento, Calif.

d.

Vicryl, Ethicon Inc, Somerville, NJ.

e.

Beaver 6400 miniblade, Beaver Visitec, Waltham, Mass.

f.

Cellugel viscoelastic, Alcon Surgical Inc, Fort Worth, Tex.

g.

Acrivet Syn 2%, Acrivet Inc, Salt Lake City, Utah.

h.

Auromedics Pharma LLC, Dayton, NJ.

i.

Infiniti Vision System Ozil Intelligent Phaco, Alcon Surgical Inc, Fort Worth, Tex.

j.

TurboSonics ultrasonic MicroTip, Alcon Surgical Inc, Fort Worth, Tex.

k.

BSS Plus irrigating solution, Alcon Surgical Inc, Fort Worth, Tex.

l.

Vazculep phenylephrine HCl injection, Éclat Pharmaceuticals, Chesterfield, Mo.

m.

Akorn Inc, Lake Forest, Ill.

n.

Alcon Laboratories Inc, Fort Worth, Tex.

o.

GenTeal Lubricant eye gel, Novartis, Pharmaceuticals Corp, East Hanover, NJ.

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