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Keywords:

  • intracapsular lens extraction;
  • lens luxation;
  • marsupial;
  • Matshchie's tree kangaroo;
  • veterinary;
  • zoo

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case report
  5. Conclusion
  6. References

An adult, female, captive, Matshchie's tree kangaroo was diagnosed with an anterior lens luxation in the right eye and a lens subluxation in the left eye. Both eyes were treated surgically with intracapsular lens extractions. A 360° rhegmatogenous retinal detachment was diagnosed 6 months postoperatively in the left eye. Aphakic vision was maintained in the right eye 9 months postoperatively. Based on family history and the lack of antecedent ocular disease, the lens luxations were presumed to be inherited and veterinarians should be aware of this condition within the captive tree kangaroo population.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case report
  5. Conclusion
  6. References

Matshchie's tree kangaroo (Dendrolagus mastchiei) is an arboreal marsupial native to Papua New Guinea. The species belongs to the family Macropodidae and is found only at high altitudes in the rainforests in the Huon Peninsula of Papua New Guinea. Matshchie's tree kangaroo is endangered due to habitat destruction and hunting. The captive population was established from 19 individuals, but only four females contribute to the majority of the offspring.[1] The captive tree kangaroo in this case report is one of the few cycling females in captivity and is, thus, an important player in the preservation of this species. Because this population is so small and importation of additional animals from the wild is restricted, the gene pool is limited and there is a significant founder effect.[1] With limited genetic diversity, the risk of inherited diseases increases and this case report documents bilateral lens luxations in a Matshchie's tree kangaroo that are suspected to be hereditary.

With the exception of one report of retinal degeneration in a captive Goodfellow's tree kangaroo (Dendrolagus goodfellowii) and a description of retinal ganglion cell topography in Doria's tree kangaroo (Dendrolagus doriana), there are no reports within the veterinary literature detailing normal ocular anatomy, pathologic ocular conditions, or the treatment of ocular disease in this species.[2, 3] We present a case of bilateral lens luxations and cataracts in a captive Matshchie's tree kangaroo that were addressed surgically with bilateral intracapsular lens extraction. Because the gene pool for this population is small, this problem may become more prevalent within the captive population in the United States.

Case report

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case report
  5. Conclusion
  6. References

A 7-year-old female captive Matschie's tree kangaroo (Dendrolagus mastchiei) was evaluated because her zookeeper and the zoo veterinarian had noted an opacity in the right eye (OD). The animal could not be handled awake and was immobilized by an intramuscular injection of a combination of medetomidine (62 mcg/kg; ZooPharm, Laramie, WY, USA), ketamine (3.9 mg/kg; Boehringer-IngelheimVetmedica Inc., St. Joseph, MO, USA), and butorphanol (0.13 mg/kg; Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) delivered via a remote delivery system (Telinject 1763 Air Pistol, Agua Dulce, CA, USA). The animal was placed in sternal recumbency for the ophthalmic exam which included diffuse illumination (transilluminator), slit-lamp biomicroscopy (SL-15; Kowa Company, Tokyo, Japan) and indirect funduscopy (Keeler Vantage Plus; Broomall, PA, USA). The intraocular pressure (IOP) was estimated using applanation tonometry (Tono-pen Vet; Reichert Inc., Depew, NY, USA). The ophthalmic examination findings included minimal direct and consensual pupillary light reflexes in both eyes (OU) and the intraocular pressures were 29 mmHg OD and 33 mmHg OS. The menace responses and dazzle reflexes were negative, and this was attributed to the deep level of sedation. A small nictitating membrane was noted, extending dorsotemporally from the ventromedial aspect of the orbit OU. There was a focal area of full-thickness corneal edema immediately ventral of axial in the right eye. The pupils were round, the irides were dark brown, and a corpora nigra was not present OU. In the right eye, the lens was anteriorly luxated and there was an early immature anterior cortical cataract. In the left eye, the lens was clear but was subluxated and an aphakic crescent was present dorsotemporally. Iridodonesis was not present in either eye and neither iris appeared to be hyperpigmented when compared to those of another tree kangaroo. The retina and optic discs were visible OU. The optic discs were similar OU and were round and pale pink in color. A small tuft of vessels was present on the surface of the optic discs OU but retinal blood vessels were not present (paurangiotic retinal vascular pattern).[4] Clinically, the appearance of the posterior segment was similar to that of the guinea pig. A tapetum lucidum was not present and the retinal pigmented epithelium appeared to be only partially pigmented creating a red hue from the underlying choroidal vessels. A complete blood cell count and biochemistry panel were performed, and the results were normal. Based on the exam findings, the animal was diagnosed with an anterior lens luxation OD and a lens subluxation OS. Although the normal range of intraocular pressures has not been established for this species, ocular hypertension was also suspected because the measured pressures were higher than the normal values reported for other marsupials.[5] Intracapsular lens extraction was recommended OU. Surgical removal of both lenses simultaneously was considered, but the decision was made to operate on each eye individually due to concern over the length of the anesthetic event needed for bilateral surgery and transport to the surgical facility. No medications were prescribed prior to surgery because the zookeepers could not safely administer topical medications.

Forty-one days after the initial exam, the animal was again immobilized by intramuscular injection using the same drug combination used for the initial exam and was then intubated and maintained under general anesthesia with isoflurane. The animal was transported under anesthesia to the surgical facility for a planned intracapsular lens extraction OD. Topical ciprofloxacin 0.3% ophthalmic solution (Akorn Inc., Lake Forest, IL, USA) and topical neomycin, polymyxin, dexamethasone solution (Alcon Lab Inc., Fortworth, TX, USA) were administered topically every 5 min (3 drops of each) during transport. An ocular exam found an absence of direct and consensual pupillary light reflexes in both eyes and intraocular pressures of 23 mmHg OD and 21 mmHg OS. Other changes from the initial exam included resolution of the previously noted corneal edema OD, progression of the cataract OD to a mature cataract, posterior movement of the lens OD into the patellar fossa with a nasal aphakic crescent (Fig. 1), enlargement of the aphakic crescent OS, and an early immature anterior cortical cataract OS. Because the intraocular pressures were elevated at the initial exam, consideration was given to the fact that the lens luxations could be secondary to chronic glaucoma and buphthalmia. If this were the case, glaucomatous retinal degeneration would be expected. Thus, a flash electroretinogram (ERG) (BPM-200; Retinographics, Inc., Norwalk, CT, USA) was performed OU. The ERGs were performed after 5 min of dark adaptation. The time permitted for dark adaption was shortened from the more typical 15 min due to a desire to limit the length of general anesthesia. The pupils were not dilated for the ERG due to the lenticular instability. Normal a- and b-waves were apparent when compared to other mammals.[7] A-wave amplitudes were 51 μV OD and 29 μV OS and the a-wave implicit times were 21 ms OD and 19 ms OS. B-wave amplitudes were 111 μV OD and 62 μV OS (b-wave reference range >100 μV in our electrodiagnostic laboratory for dogs; ERG values for normal tree kangaroos have not been established) and the b-wave implicit times were 44 ms OD and 39 ms OS. The lower b-wave amplitude OS was attributed to the lack of pupillary dilation although retinal degeneration could not be definitively excluded. The right pupil was more dilated than the left presumably due to mechanical interference from the luxated lens.

image

Figure 1. Photograph of the right eye immediately prior to intracapsular lens extraction. Note the mature cataract and temporal aphakic cresent.

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The right eye was aseptically prepared for surgery. Atracurium (0.1 mg/kg; Sagent Pharmaceuticals, Inc., Schaumburg, IL, USA) was administered intravenously to centralize the globe, and the animal was mechanically ventilated; this single dose provided adequate globe centration for the procedure. An intracapsular lens extraction was performed using an operating microscope (OPMI VISU 200; Zeiss, Germany). A 7 mm lateral canthotomy was created to increase globe exposure. A dorsal clear corneal approach was used, and a 150° partial depth corneal incision was made with a 6900 blade (Eagle Labs, Cucamonga, CA, USA). The incision was approximately 1.5 mm from the limbus. A full-thickness stab incision was made in the center of the corneal incision with a 2.8 mm keratome. Right and left handed corneoscleral scissors were used to extend the corneal incision in both directions. The iris promptly herniated through the incision and was replaced with a small amount of viscoelastic. A partial-thickness corneal stay suture was placed using 8-0 Vicryl (Ethicon, Somerville, NJ, USA), and it was used to retract the corneal incision while a 2-mm curved nitrous oxide cryoprobe was affixed to the anterodorsal lens capsule with an approximately 3-mm ice ball. The lens was gently extracted with the cryoprobe. There were no intact attachments between the posterior lens capsule and the anterior vitreous. An open-sky anterior vitrectomy was planned, but no vitreous was identified within the anterior chamber and the anterior vitreal face appeared to be well formed. The anterior chamber was reformed with viscoelastic (Hylartin V; Advanced Medical Opticsc Uppsala AB, Uppsala, Sweden). The corneal incision was closed with a simple continuous pattern using 8-0 Vicryl (Ethicon). The closure was complicated by continual prolapse of the iris through the corneal incision. Despite intermittent injections of viscoelastic to reposition the iris, the iris was traumatized repeatedly during the corneal closure resulting in intraocular hemorrhage. The bleeding was controlled via viscoelastic tamponade, and the viscoelastic was not removed from the anterior chamber. 25 mcg of tissue plasminogen activator (Prescription Center, Fayetteville, NC, USA) was injected intracamerally at the conclusion of surgery. The lateral canthus was closed with a simple interrupted pattern using 5-0 Vicryl Rapide (Ethicon). Because postoperative medications would be limited to oral medications due to the animal's intractability, 25 mg of amikacin (Fort Dodge Animal Health, Fort Dodge, IA, USA), 50 mg of cefazolin (WG critical care LLC., Paramus, NJ, USA), and 4 mg of triamcinolone acetonide (Bristol-Myers Squibb Co., Princeton, NJ, USA) were injected subconjunctivally. One drop of dorzolamide/timolol solution (Hi-tech Pharmacal Co., Inc., Amityville, NY, USA) followed by a 1/8 inch strip of neomycin, polymixin, dexamethasone ointment (Bausch & Lomb Inc., Tampa, FL, USA) were administered topically. A temporary tarsorrhaphy was placed to protect the globe using two horizontal mattress sutures of 5–0 silk (Ethicon) over rubber band stents. The animal was then transported back to the zoo and recovered from general anesthesia in a small enclosure. Postoperative care consisted of oral enrofloxacin (5 mg/kg PO BID; Bayer Healthcare LLC, Shwanee Misson, KS, USA) for 14 days and a tapering course of oral prednisone for 28 days (initial dose of 0.4 mg/kg PO BID; West-Ward Pharmaceutical Corp., Eatontown, NJ, USA). The animal was kept alone in a small enclosure within the zoo's veterinary hospital for the first 4 weeks following surgery and then was moved to a moderately sized enclosure for a total of 4 months.

The tree kangaroo was immobilized using an intramuscular injection of the previously utilized drug combination and recheck examinations were performed 8 days, 16 days, 3 months, 4 months, and 9 months postoperatively. Each recheck exam was similar to the initial exam and included slit-lamp biomicroscopy, tonometry, indirect funduscopy, and fluorescein staining. The temporary tarsorrhaphy was replaced due to loosening of the sutures 8 days postoperatively and was removed 16 days postoperatively. Because topical corticosteroids could not be safely administered and postoperative uveitis was expected, an additional subconjunctival injection of 4 mg of triamcinolone (Bristol-Myers Squibb Co.) was administered 8 days postoperatively. The IOP remained within the normal range for marsupials at each recheck examination (10–23 mmHg).[4] Aqueous humor flare was not present at any of the postoperative examinations. Vitreal hemorrhage was present immediately postoperatively (presumably from intraoperative iridial hemorrhage), 8 and 16 days postoperatively but had resolved 3 months postoperatively. Vitreal degeneration was present at the 3, 4, and 9 month postoperative exams, and a small strand of vitreous was noted in the anterior chamber at the 4 and 9 month postoperative exams. The corneal incision healed with a moderate amount of scarring and the retina and optic nerve head appeared unchanged from their preoperative appearance at each postoperative exam.

Three months after the intracapsular lens extraction, OD the animal was again anesthetized and transported to the surgical facility for an intracapsular lens extraction OS. The exam in the left eye was unchanged from the previous exam, and the IOP was 21 mmHg. The left lens was extracted in a similar manner to the right. However, the clear corneal incision was placed 3 mm from the limbus which prevented prolapse of the iris through the incision. The surgery was uncomplicated until the corneal closure was near completion at which point the animal developed severe blepharospasm due to an inappropriate depth of anesthesia and loss of the neuromuscular blockade. The globe partially proptosed and the eyelid speculum was removed and gentle pressure was applied to the globe until the patient was re-anesthetized. Following this event, there was a moderate amount of anterior chamber hemorrhage. A partial tarsorrhaphy was placed with one horizontal mattress suture and topical, and subconjunctival medications were administered in an identical manner to the right eye. Oral enrofloxacin (5 mg/kg PO BID for 14 days) and oral prednisone (initial dose of 0.4 mg/kg tapered over 28 days) were administered postoperatively.

Recheck examinations were performed 16 days, 1 month, and 6 months postoperatively. The temporary tarsorrhaphy was removed 16 days postoperatively. The IOPs at all recheck examinations were normal and ranged from 13 to 18 mmHg. A superficial, 2 mm × 1 mm corneal ulcer was present ventral to the incision at the 16 day postoperative exam. This was addressed with subconjunctival injections of amikacin (25 mg, 0.1 mls) and cefazolin (50 mg, 0.1 mls). The ulcer had resolved at the next exam but several, pinpoint mid-stromal facets were present immediately ventral to the corneal incision. Trace aqueous humor flare was present at every recheck examination; postoperative subconjunctival injections of corticosteroids were not administered due to the corneal ulceration. A peripheral rhegmatogenous retinal detachment was noted 1 month postoperatively. The retinal detachment was located at the ora ciliaris retinae and extended from the 10 to 12 o'clock position. Diode laser retinopexy was considered but not pursued because the animal was losing weight and had developed diarrhea, and another lengthy general anesthetic event was deemed too risky. At the final recheck exam 6 months following the operation OS, there was a small blood clot in the anterior chamber OS and a 360 degree rhegmatogenous retinal detachment. The animal's weight loss and diarrhea resolved with cessation of the oral prednisone and transfaunation.

At the final exam, the zookeepers reported that the animal appeared to be visual and that, with the exception of turning her head to examine objects of interest with the right eye, she had no behavior changes that would suggest a decrease in vision. In addition, she was able to avoid objects at high speeds, and no difference had been noted in her ability to climb and jump from her preoperative abilities.

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case report
  5. Conclusion
  6. References

Dislocation of the lens from the patellar fossa is a relatively common problem encountered in veterinary ophthalmology. Lens luxations and subluxations occur when there is an abnormality in the ciliary zonules which form the normal suspensory apparatus of the lens. Lens luxations may be classified as primary, in which no antecedent ocular disease is present, secondary, congenital, or traumatic.[6] Familial canine primary lens luxations are encountered frequently and, recently, a mutation in a gene located on canine chromosome 3 has been shown to cause primary lens luxation in several breeds.[8] Familial lens luxations (ectopia lentis) in human patients have also been documented, often in association with systemic disorders.[9-11] Secondary lens luxations typically occur secondary to cataracts, uveitis, and chronic glaucoma with buphthalmia. Congenital and traumatic lens luxations are rarely encountered in veterinary medicine.[12-15]

In the case reported here, the etiology of the lens luxations was assumed to not be congenital or traumatic based on the history. Lens luxation secondary to primary glaucoma was considered as the intraocular pressures were elevated OU at the initial exam. However, the globes did not appear to be buphthalmic when compared to another tree kangaroo in the exhibit and the IOPs were normal at every exam following the initial one. As the cataract in the right lens was small and no cataract was present in the left lens at the initial exam, it was unlikely that the lens luxations were secondary to cataracts. There was also no evidence on the exam to support lens luxation secondary to chronic anterior uveitis. Finally, the family history of this animal strongly suggested an inherited disorder. The animal's mother and sister had both suffered anterior lens luxations with no known antecedent ocular disease. The mother of this animal reportedly developed blinding glaucoma secondary to bilateral anterior lens luxations. The sister of the animal reported here also had bilateral intracapsular lens extractions.

The technique used to extract the lenses in this animal was adapted from the method in which luxated lenses are routinely removed from canine patients.[15] However, the positioning of the corneal incision in the clear cornea adjacent to the limbus, as would be performed in a canine patient, resulted in repeated prolapse of the iris through the incision with subsequent injury to the iris and intraocular hemorrhage. In the second operation, the corneal incision was placed several millimeters away from the limbus which remedied the problem of iris prolapse through the corneal wound and this location is recommended for lens extractions in this species.

Complications following intracapsular lens extractions are not uncommon and include glaucoma, retinal detachment, uveitis, and wound dehiscence.[15] Potential causes for the retinal detachment in this animal's left eye include a small preoperative tear that was unrecognized and enlarged postoperatively, intraoperative injury when the animal temporarily woke up during surgery, disruption of the anterior hyaloid face, intraoperative vitreal loss, vitreal hemorrhage, and vitreal liquefaction.[16-18] This case demonstrates that, similar to the dog, postoperative retinal detachment is a concern in this species following an intracapsular lens extraction. In addition, this species can be difficult to medicate and examine without chemical restraint which makes postoperative care challenging. The use of perioperative subconjunctival injections was useful in this animal as an alternative to topical medications, which could not be safely administered.[19]

There is limited published information available on the normal ocular anatomy of this species. Based on the exam findings in this individual, the basic ocular anatomy of the tree kangaroo includes a round pupil, an absence of a corpora nigra, a paurangiotic retinal vascular pattern, and a small nictitating membrane. In retrospect, additional useful anatomic information could have been obtained by measuring the limbal to limbal corneal diameters with calipers and by measuring the anterior to posterior length of the globe using ultrasound.

The tree kangaroo in this case report has played and is expected to continue to play, an integral role in the captive breeding program for this species. If the lens luxations in this animal are inherited, as we suspect, spontaneous lens luxations may become more prevalent within the captive tree kangaroo population and zoo veterinarians and veterinary ophthalmologists should be aware of this condition.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Case report
  5. Conclusion
  6. References
  • 1
    McGreevy TJ, Dabek L, Gomez-Chiarri M et al. Genetic diversity in captive and wild Matschie's tree kangaroo (Dendrolagus matschiei) from Huon Peninsula, Papua New Guinea, based on mtDNA control region sequences. Zoo Biology 2009; 28: 183196.
  • 2
    Schmidt RE, Toft JD. Ophthalmic lesions in animals from a zoologic collection. Journal of Wildlife Diseases 1981; 17: 267275.
  • 3
    Hughes A. A comparison of retinal ganglion cell topography in the plains and tree kangaroo. Journal of Physiology 1975; 244: 6163.
  • 4
    De Schaepdrijver L, Simeons P, Lauwers H et al. Retinal vascular patterns in domestic animals. Research in Veterinary Science 1989; 47: 3442.
  • 5
    Labelle AL, Low M, Hamor RE et al. Ophthalmic examination findings in a captive colony of western gray kangaroos (Macropus fuliginosus). Journal of Zoo and Wildlife Medicine 2010; 41: 461467.
  • 6
    Ekesten B. Ophthalmic examination and diagnostics. Part 4: electrodiagnostic evaluation of vision. In: Veterinary Ophthalmology, 4th edn. (ed. Gelatt KN) Blackwell Publishing, Iowa, 2007, 520535.
  • 7
    Foster SJ, Curtis R, Barnett KC. Primary lens luxation in the Border Collie. Journal of Small Animal Practice 1986; 27: 16.
  • 8
    Farias FHG, Johnson GS, Taylor JF et al. An ADAMTS17 splice donor site mutation in dogs with primary lens luxation. Investigative Ophthalmology & Visual Science 2010; 51: 47164721.
  • 9
    Dureau P. Pathophysiology of zonular diseases. Current Opinions in Ophthalmology 2008; 19: 2730.
  • 10
    Neuhann TM, Artelt J, Neuhann TF et al. A homozygous microdeletion and ADAMTSL4 in patients with isolated ectopia lentis: evidence of a founder mutation. Investigative Ophthalmology & Visual Science 2011; 52: 695700.
  • 11
    Morales J, Latifa A-S, Khalil DS et al. Homozygous mutations in ADAMTS10 and ADAMTS17 cause lenticular myopia, ectopia lentis, glaucoma, spherophakia, and short stature. American Journal of Human Genetics 2009; 85: 558568.
  • 12
    Grahn BH, Storey E, Cullen CL. Diagnostic ophthalmology. Canadian Veterinary Journal 2003; 44: 427430.
  • 13
    Molleda JM, Martin E, Ginel PJ et al. Microphakia associated with lens luxation in the cat. Journal of the American Animal Hospital Association 1995; 31: 209212.
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    Aguirre GD, Bistner SI. Microphakia with lenticular luxation and subluxation in cats. Veterinary Medicine, Small Animal Clinician 1973; 68: 498500.
  • 15
    Wilkie DA, Colitz CMH. Surgery of the canine lens. In: Veterinary Ophthalmology, 4th edn. (ed. Gelatt KN) Blackwell Publishing, Iowa, 2007; 888931.
  • 16
    Vainisi SJ, Wolfer JC. Canine retinal surgery. Veterinary Ophthalmology 2004; 7: 291306.
  • 17
    Mitry D, Fleck BW, Wright AF et al. Pathogenesis of rhegmatogenous retinal detachment: predisposing anatomy and cell biology. Retina 2010; 30: 15611572.
  • 18
    Narfström K, Petersen-Jones S. Diseases of the canine ocular fundus. In: Veterinary Ophthalmology, 4th edn. (ed. Gelatt KN) Blackwell Publishing, Iowa, 2007, 9441025.
  • 19
    Schoenwald RD. Ocular pharmacokinetics. In: Textbook of Ocular Pharmacology, 1st edn. (eds. Zimmerman TJ, Kooner KS, Sharir M et al. ) Lippincott-Raven Publishers, Philadelphia, 1997, 119138.