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Convergent strabismus in a whiteBengal tiger

ME BERNAYS and RIE SMITHAnimal Eye Services, Kessels Road Veterinary Hospital, Macgregor, Queensland 4109

A white Bengal tiger was noted to have a convergent strabismus with poor visionsince a cub. The tiger and a littermate with normal colouring and apparently normaleyes were anaesthetised for comparative ocular examination. A fundus typical ofcolour-dilute cats and dogs was noted in the white tiger. Except for strabismus, noabnormalities were observed. Electroretinography showed similar retinal function inboth tigers. Possible causes of strabismus considered were an adaptation to genet-ically determined abnormal visual pathways related to lack of pigment, abnormalitiesof the abducent nerves and mechanical restricting conditions of the medial rectusmuscles.Aust Vet J 1999;77:152-155Key words: Tiger, convergent strabismus, colour-dilute, albinism, neural pathways, lateral geniculate body,lamina A1, lamina C1.

LGN Lateral geniculate nucleus

Figure 2. Normal orange-coated littermateat 12 months of age.

Figure 1. White tiger at 12 months of age,showing a convergent strabismus.(Courtesy of P Martin-Vegue).

A2-year-old female white Bengaltiger had been acquired as a cubat 5 weeks of age. The head

keeper had noted her eyes were normalat that time. At about 8 weeks, a subtlebilateral convergent strabismus wasnoted. Over the next 10 months, stra-bismus became progressively moreobvious (Figure 1). No further deterio-ration was noticed after 12 months ofage. The handlers had observed that attimes, in addition to the strabismus, thetiger would run in a circuitous fashionto get from one point to another. It hadalso been observed tilting its head inone direction whilst looking at anobject in the opposite direction. Wewere asked to examine the white tiger’seyes to determine if there were anyobvious abnormalities that mightexplain its appearance and behaviour. A

normal orange-coated littermate wasexamined for comparison (Figure 2).

Ocular examinationAnaesthesia was induced by darting

with zolazepam and maintained withhalothane using a circle system. Theeyes of both tigers were examined usingbinocular indirect ophthalmoscopy(Heine Omega 180 with a 20D hand-held lens) and slit-lamp biomicroscopy(Kowa SL14). Intraocular pressure wasassessed using a Tonopen (Mentor Inc).An OG3MI 3 mirrored goniolens(Ocular Instruments) was used to assessiridocorneal angles. A fundus camera(Kowa Genesis) was used to photo-graph retinal fundi. Electroretinogramswere recorded using standard protocolsin light conditions (photopic) and afterdark adaptation (scotopic) with a

EDITOR

DAVID WATSON

ADVISORY COMMITTEE

AVIANLUCIO FILIPPICH

EQUINEDAVID HODGSON

OPHTHALMOLOGYJEFF SMITH

PRODUCTION ANIMALS JAKOB MALMO

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ZOO/EXOTIC ANIMALS LARRY VOGELNEST

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Aust Vet J Vol 77, No 3, March 1999 153

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Retinographics BPM-100 systemconnected to a notebook computer withanalysis software. The stimulus intensitywas set to measure a mixed rod and coneresponse after dark adaptation.

The white tiger was examined first: noasymmetry in structure was noted withthe fellow eye. The eyelids were normalwith light pigment creating a pale browncolour. The lateral aspect of the bulbarconjunctiva showed light pigmentationoccurring in horizontal streaks, andarising approximately 5 to 10 mmcaudal to the limbus. This occurred in aregion of conjunctiva which was notwell covered by lateral eyelid or canthus(Figure 3). There were no significantfindings on examination of the cornea,anterior chamber, iris, lens or vitreous.Iris colour was pale cream to slightlyblue. The iridocorneal angle was classi-fied as open with large well-spaced pecti-nate ligaments bridging the spacebetween the iris root and posteriorlimbal cornea. The pupil margin wascircular, and an irregular oscillatorypattern of pupil constriction was notedimmediately after induction of anaes-thesia and for about 20 min after topicalinstillation of 1% tropicamide (Mydri-acyl). The intraocular pressure was 21mm Hg in the right eye and 18 mm Hgin the left eye.

The fundus was very similar inappearance to that normally observed incolour-dilute small domestic felines. Thehead of the optic nerve was round andpale cream with pairs of vesselsemanating from the edge (Figure 4). Thetapetum was roughly triangular in shapeand green to yellow. There was a smalltransition zone between the tapetumand the nontapetum associated withgradual loss of tapetal reflection. Thisarea had a blotchy red-green appearance.Large, radiating, almost parallelchoroidal vessels were observed in thenontapetum because of absence ofpigment in the retinal pigment epithe-lium (Figure 5).

The electroretinogram showed aphotopic response amplitude of 54.7 µV(recording mainly cone photoreceptors)that was significantly larger thannormally seen in small domestic cats.This was deemed to be due to summa-tion of a larger absolute number ofphotoreceptors in a larger eye. Thelatency of 11.2 ms was similar to thatseen in small domestic cats, as summa-

tion should not affect latency. After 15min dark adaptation, a scotopicresponse amplitude of 577 µV wasrecorded (recording mixed rod and conephotoreceptors but mainly rods becauseof their dominance). This was alsomarkedly larger than the normalresponse seen in a small domestic cat.Latency was 17 ms. A 30 Hz flicker testwas performed; this showed a normalmixed rod-cone response without fusion.

The ‘normal’ orange littermate wasexamined using the same anaestheticregimen for restraint. The eyelidmargins were well pigmented with darkblack colouration. The lateral bulbarconjunctiva showed similar but muchdarker pigment patterning than that inthe white tiger. There were no signifi-cant findings on examination of thecornea, anterior chamber and iris. Theiris colour was a pale yellow. As observedin the white littermate, the iridocornealangle was classified as open with largewell-spaced pectinate ligaments bridging

the space between the iris root andsclera. A small area of cataractous changewas noted in the anterior subcapsularcortex of the right eye. The significanceor possible aetiology of this cataract wasnot determined. Intraocular pressurewas 21 mm Hg in the right eye and 22mm Hg in the left. The tapetal fundusin both eyes had similar appearance tothat of the white tiger, but thenontapetum was well pigmented withchoroidal vessels not readily visible(Figure 6).

The electroretinogram showed aphotopic response amplitude of 51.9 µVand latency of 11.2 ms. After 15 mindark adaptation, a scotopic responseamplitude of 548 µV with latency of19.3 ms was recorded. A similar flickerresponse at 30 Hz to that recorded forthe white tiger was also noted. The simi-larities between the curves for the twotigers confirmed that visual defects wereprobably not related to differences inretinal function in the white tiger.

Figure 3. Right eye of the white tiger.Note pale brown pigmentation of thevery exposed lateral bulbar conjunctivadue to the strabismus, and the pale blueiris.

Figure 4. Central tapetal region of thewhite tiger. Note the appearance of opticdisc and radiating vessels is similar tothat of small domestic felines.

Figure 5. View of the junction betweenthe tapetum and nontapetum in thewhite tiger. Note the visible choroidalvessels due to lack of pigment in theretinal pigment epithelium.

Figure 6. View of the junction between thetapetum and the nontapetum in thenormal tiger. Pigment in the retinalpigment epithelium obscures the view ofthe choroid in the nontapetal area.

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Differential diagnosisAs differential diagnoses for the stra-

bismus observed in the white tiger, thefollowing possibilities were considered:

● an adaptation to genetically deter-mined abnormal visual pathways.

● an ocular motor neural abnormalityequally affecting both abducentnerves (sixth cranial nerve, CN VI).This diagnosis was excluded becauseof the improbability of such a bilat-eral lesion and the difficulty of con-firming pure CN VI abnormalitieson both practical and neurophysio-logical grounds (see discussion).

● a mechanical restricting conditionequally affecting both medial rectusmuscles. This was also considered tobe unlikely, although specific forcedduction tests to check for entrap-ment or fibrosis of the medial rectusmuscles were not performed.

DiscussionA bilateral abnormality of CN VI

without asymmetry would have to havea localised lesion in the rostrodorsalmedulla adjacent to the midline wherethe nuclei for each side are in close prox-imity. It was not possible to test in isola-tion the function of the retractor bulbimuscles, which are also supplied by CNVI, because the eyeball retractionresponse needs to be performed in aconscious animal with eyelids retractedso that the eyeball can be observedretracting in response to a menace (CNII) or a corneal sensory (CN V)response. In addition it is thought thatthe eyeball retraction response is not aspecific test for efferent CN VI functionbecause all extraocular muscles maycontract as part of this response. Itshould therefore be regarded as a test formixed function of the ventral, medialand dorsal rectus and ventral obliquemuscles innervated by CN III, the supe-rior oblique muscle (CN IV) and thelateral rectus and retractor bulbi muscles(CN VI).

An active forced duction test can beused to determine if there is asymmetryin the mobility of opposing extraocularmuscles such as medial and lateraloblique muscles. If length or mobility ofthe medial rectus muscle was affected,then an active forced duction test wouldreveal a lateral rectus muscle whichcould pull the eyeball caudally but not

rotate it laterally. Active forced ductionwas not performed because the tiger wasexamined under general anaesthesia.There was no indication, however, ofrestriction of eyeball movement duringexamination under anaesthesia.

White tigers have been known tooccur in nature for some time. Theabnormality of pigmentation occurs in apattern which suggests autosomal reces-sive inheritance. White tigers have thegrey-brown to black stripes seen innormal tigers, but the normal yellowstriping is replaced by an off-white tocream colour. These tigers are homozy-gous for an allele of the ‘albino’ serieswhich is very similar to the ‘Himalayan’gene which occurs in pointed cats suchas the Siamese or Colourpoint Persian.The allele may be more like anotherallele of the ‘albino’ series, referred to as‘chinchilla’ in its effect on pigment.They have reduced pigment in the iris,which is blue, and a distinct lack ofpigment in the nontapetal fundus.While convergent strabismus is knownto occur in humans, cats, rats, rabbits,ferrets, minks and wallabies that havedeficiencies of pigment in the retinalpigment epithelium,1 there is only oneprevious report of a white tiger with thisdefect.2 On the basis of the history andclinical findings, it was considered thatthe tiger in our report was most likely tohave strabismus related to abnormalvisual pathways.

Siamese cats, in which most researchhas been done, have a number of retino-geniculate projections from thetemporal aspect of the retina (the arealateral to the area centralis and relatedvertical meridian) which decussate at theoptic chiasm to the contralateral LGN.These projections arise from about thefirst 20° of the temporal retina and innormal cats would project to the ipsilat-eral side. They synapse in the contralat-eral LGN layers A1 and C1 whichwould normally receive projections fromthe temporal retina on the ipsilateralside. This results in abnormal lamina-tion of the lateral geniculate body. Theabnormal lamination can be demon-strated by routine histochemicalstaining, by nerve fibre degenerationstudies following unilateral enucleation,and by microelectrode recording ofLGN activity in anaesthetised cats withnarrow beam light stimulation.3,4 Otherabnormalities which have been shown

include differences of ganglion celldensity around the area centralis ofSiamese cats,5 and an area of widenedtransition between ipsilaterally andcontralaterally projecting ganglion cellaxons6,7 compared with normal cats.8,9

Because of the abnormal projections,representative parts of the visual fieldswhich would ‘line-up’ between layers Aand A1 are misaligned, with a segmentof the ipsilateral visual field inserted inlayer A1, where a section representingthe contralateral field should normallyoccur. This results in a loss of binocularvision.

Two types of Siamese cats have beenidentified and named the Boston typeand the Midwestern type10-12 dependingon how these inputs to the LGN aresubsequently processed by projections tothe cerebral cortex. The two types alsodiffer in morphology of LGN lamina-tion as well.11,12

The Midwest cat appears to suppressthe abnormal lamina A1 input to thevisual cortex, so that only informationfrom layers A and C is used in visualperception of the external environment.This probably means that binocularity islost. This type is known to have anormal visual field when both eyes areopen, but when one eye is closed theperceived visual field is 90°, representingonly that portion of the total monocularfield (normally 135°) viewed from thenasal retina.12

The Boston cat has rearranged theabnormal inputs to the cortex from layerA1, reversing them and inserting themat one end of the projections of layer Ato give an extended, orderly and sequen-tial representation of the visual fieldaround the boundary of areas 17 and 18of the visual cortex. In these cats, orderlyrepresentation in the visual cortex occurseven when the kitten is raised from birthwith the eyelids of both eyes suturedclosed. This suggests that the develop-ment of the Boston pattern is indepen-dent of visual experience and likely isdeveloped at birth.

The strabismus is thought to occur asthe result of attempts by the visualcortex to match respective parts of thevisual field as perceived by each eye. Thevisual cortex presumably directs extraoc-ular muscles via connections with thenuclei of CNs III, IV and VI to adoptthe position of medial strabismus in anapparently unsuccessful attempt to

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match parts of the visual field to achievebinocularity. Siamese kittens are bornwith a divergent strabismus, as arenormal kittens. Over the first 3 monthsof life, the visual axes move to firstparallel each other, then continuemoving until they become convergent.The abnormality is highly variable in itsseverity in different Siamese, but it is feltthat the most severely affected cats havethe greatest degree of abnormalcrossover.13

In the only previous report on a whitetiger, Guillery and Kaas noted similarunusual LGN lamination patterns tothat seen in Siamese cats.2 While thedead tiger referred to in their report wasthought to have had eyes whichappeared to be aligned normally, itssurviving sister at that time had markedstrabismus.

Because of the invasive nature of theexperimental methods required toconfirm how optic nerve axon crossoveroccurs in the live animal, and how thevisual cortex deals with this resultingcontradictory information from theLGN, we cannot be certain how visual

information is processed in this whitetiger. However, based on the demon-strated lack of pigment noted onfundoscopy, and the apparent normalityof the eyes in all other respects, it isconcluded that the tiger probably hasabnormal vision and strabismus relatedto abnormal retinogeniculate crossoverand abnormalities in visual corticalprocessing.

AcknowledgmentsThe authors would like to thank the

handlers at Tiger Island, Dreamworld, inparticular the head keeper, Mr PatrickMartin-Vegue, for his kind assistance inproviding background material, and DrLarry Vogelnest of Taronga Park Zoo,Sydney, for anaesthetising the tigers.

References1. Guillery RW. Visual pathways in albinos. Sci Am1974;230:44-54.2. Guillery RW, Kaas JH. Genetic abnormality ofthe visual pathways in a ‘white’ tiger. Science1973;180:1287-1288.3. Guillery RW. An abnormal retinogeniculateprojection in Siamese cats. Brain Res1969;14:739-741.

4. Guillery RW, Kaas JH. A study of normal andcongenitally abnormal retinogeniculate projectionsin cats. J Comp Neurol 1971;143:73-100.5. Stone J, Rowe MH, Campion JE. Retinal abnor-malities in the Siamese cat. J Comp Neurol1978;180:773-782.6. Stone J, Rowe MH, Campion JE. The nasotem-poral division of retina in the Siamese cat. J CompNeurol 1978;180:783-798.7. Cooper ML, Pettigrew JD. The retinothalamicpathways in Siamese cats. J Comp Neurol1979;187:313-348.8. Cooper ML, Pettigrew JD. The decussation ofthe retinothalamic pathway in the cat, with a noteon the major meridians of the cat’s eye. J CompNeurol 1979;187:285-312.9. Illing RB, Wässle H. The retinal projection to thethalamus in the cat: a quantitative investigationand a comparison with the retinotectal pathway. JComp Neurol 1981;202:265-285.10. Hubel DH, Wiesel TN. Aberrant visual projec-tions in the Siamese cat. J Physiol 1971;218:33-62.11. Schatz C. A comparison of visual pathways inBoston and Midwestern Siamese cats. J CompNeurol 1977;171:205-228.12. Kaas JH, Guillery RW. The transfer ofabnormal visual field representations from thelateral geniculate nucleus to the visual cortex inSiamese cats. Brain Res 1973;59:61-95.13. Blake R, Crawford MLJ. Development of stra-bismus in Siamese cats. Brain Res 1974;77:492-496.

(Accepted for publication 21 October 1998)

Inguinal herniation after equine castration

Eventration is a serious complication of castrating horses. Just how serious it is was studied by a team ofresearchers from University of California, Davis. They analysed the records of 18 horses treated during

a 10 year period. The number of horses did not allow conclusions about breed predilection, but Standard-breds are believed to be relatively susceptible. Eventration followed castration with a median interval of 2 h.Two horses developed herniation later: one at 38 h and one 1 week after castration. The jejunum was themost common organ to herniate.

Eight horses were treated with ventral midline laparotomy and six with inguinal approach only. Fourhorses were operated first through an inguinal approach and later with laparotomy. Fourteen horses under-went resection and anastomosis of the intestine.

Postoperative complications arose in 14 cases. The most common were colic (13), peritonitis (5) andileus (4). Thirteen horses were discharged home. The median survival time was 3.5 months (range 24 h to8 years). The most common reason for euthanasia during follow-up was recurrent colic (8 cases). Six ofthese were necropsied and found to have extensive intestinal adhesions.

Short-term survival rate was 72% and long-term rate 40%. Three factors worsened survival rate signifi-cantly: treating the prolapse initially through inguinal approach, bowel resection and the length of affectedintestine. Of these factors the use of the inguinal approach was by far the most important, to the point thatthe authors do not recommend it for treatment of postcastration eventration. Only 40% of horses treatedwith it were discharged, whereas 72% of horses that underwent laparotomy went home.

Castration complications are the single largest source of malpractice claims for equine practitioners in theUSA. The findings of this study facilitate prognostication in cases of postcastration eventration.

Thomas HL, Zaruby JF, Smith CL, Livesey MA. Postcastration eventration in 18 horses: the prognostic indicators for long-term survival (1985-1995). Can Vet J 1998;39:764-768.