0749-0720/94 $0.00 + .20
UPDATE ON LLAMA MEDICINE
OPHTHALMOLOGY Juliet R. Gionfriddo, DVM, MS
Despite the continued popularity of South American camelids, little research has been done on the anatomy, physiology, or pathology of the llama eye. Much of the information presented here was drawn from a relatively small number of case reports and other publications, many of which concern ocular disease in alpacas, guanacos, and vicunas. Another source of information was anecdotal reports offered by veterinary ophthalmologists regarding their diagnoses of ocular diseases and their successes with camelid ocular surgeries. These reports have been included in this article to help document the frequencies and types of ocular diseases to which camelids are susceptible and the types of treatments that have been used. Also included are data regarding all llama eye cases presented to Colorado State University Veterinary Teaching Hospital (CSU-VTH) during 1980 through 1992. These data are summarized in Table l. Although the four South American camelid species (llamas, alpacas, vicunas, and guanacos) are dosely related (three are congeneric), the extent to which their anatomies, susceptibilities to disease, and hereditary problems differ is unknown. Apparent ocular similarities among the species, however, suggest they probably share many common aspects in ophthalmic biology. This review therefore covers all four South American camelid species.
EXAMINATION OF THE CAMELID EYE
A thorough examination of the camelid eye is an important part of routine health checks and in cases in which ocular or orbital disease is suspected. Because several systemic diseases in llamas have ocular manifestations, the eyes of all sick animals should be examined carefully. Ocular examination should be conducted in a quiet location where lighting can be reduced. The amount and type of restraint needed for examination depends on the individual animal. Facial contact may elicit rapid head movement and spitting or kicking. Restraint in stocks therefore is advisable. In most cases,
From the Eye Clinic for Animals, Overland Park, Kansas
VETERINARY CLINICS OF NORTH AMERICA: FOOD ANIMAL PRACTICE VOLUME 10 • NUMBER 2 • JULY 1994
Table 1. OCULAR DISEASES DIAGNOSED IN 123 LLAMAS AT COLORADO STATE UNIVERSITY VETERINARY TEACHING HOSPITAL DURING 1980-1992 Diseased Structure or Condition
32 20 19 16 11 11 10 9 7 4 2 2 1 1 145
22 14 13 11 8 8 7 6 5 3 2 2 1 1 100
Cornea Conjunctiva Retina/optic nerve Lens Blindness (crias) Anterior uveitis Nasolacrimal Eyelids Sclera Vitreous Amblyopia Glaucoma Anterior chamber Congenital nystagmus Total
the head may be controlled gently by placing it over a padded bar (taking care to rest the head on the mandibles rather than the larynx) and wrapping a towel behind the ears.ll Some individuals require chemical sedation (e.g., butorphenol 0.02-0.04 mg/kg) to control head movement. After restraining the camelid, the eye is inspected. The position and size of the globes, their relationship to facial structures, and the position and movement of the eyelids should be noted. The orbital rim, globe, and periocular area should be palpated gently to check for any swellings or masses. Next, a systematic evaluation of the eye is undertaken. This includes examination of the anterior segment under magnification with a head loupe and strong light source or a biomicroscope. Pupillary light reflexes, menace reflexes, and blink reflexes may be tested at this time. Fundoscopy may be done with a direct ophthalmoscope or with an indirect system using a 20 D aspheric lens and a transilluminator. Dilation of the pupil with 1% tropicamide greatly facilitates fundus evaluation. Dilation usually takes 20 to 45 minutesY After a thorough ocular examination, ancillary tests may be performed. If a culture is desired, it should be taken prior to instilling anesthetic, mydriatic, or fluorescein stain in the eye. Conjunctival or corneal cultures may be taken with a sterile cotton swab or flame-sterilized Kimura spatula. Schirmer tear test (SIT) strips usually are well tolerated by llamas, and a mean SIT value of 19 mm/ minute has been reported. ll Measurement of intraocular pressure (lOP) in llamas is difficult with a Schiotz tonometer because of the elaborate head positioning needed to obtain accurate results with this instrument. A Tonopen applanation tonometer is easy to use on llamas and their average lOP taken with it is 14 mm HgY
ANATOMY OF THE NORMAL CAMELID EYE
With a few notable exceptions, the anatomy of the normal camelid eye is similar to that of other livestock species. Camelid eyes are very large in relation
to head size, making their appearance prominent. Llama globes, in fact, are only slightly smaller than those of horses or cattle, whose heads are much largerY The large camelid cornea covers most of the palpebral fissure, which makes the sclera difficult to see in the normal resting state and adds to the apparent ocular prominence. In addition, the limbal conjunctiva usually is pigmented, so little "white" shows around the cornea. The eyelids adhere tightly to the globe and must be retracted manually to examine the conjunctiva. Numerous long eyelashes frequently are present on the upper and lower eyelids, and three sets of long, prominent vibrissae often are seen. 11 Unlike other domestic animals, camelids lack meibomian gland duct openings on the eyelid margins. l1 The outer, oily tear layer (produced by meibomian glands in most mammalian species) probably is produced by sebaceous glands on the lacrimal caruncle in llamas. These sebaceous glands are present in camels (Camelus spp.), close relatives of llamas, and probably are present in the llama. 6,11 The lacrimal puncta of llamas are fairly large and are located several millimeters inside the edge of the upper and lower eyelids near the medial canthus. The edge of the nictitating membrane can be seen in the resting state and may be pigmented or unpigmented. Retropulsion on the globe moves the nictitans across the eye in a medial-to-Iateral direction. A prominent T-cartilage and a large gland of the nictitans can be seen through the thin conjunctiva covering the third eyelid. II Iris pigmentation in the llama varies from dark brown to light brown to nonpigmented (blue or glass eye).s Specks of dark pigment may be present in lighter irises and streaks of blue (nonpigmented areas) may be present in darker irises. There are two reported cases of blue-eyed llamas that were deaf. Although the genetics are not completely understood, this is thought to be a hereditary problem in llamas and breeding for the blue-eyed trait is strongly discouraged (Johnson LW, personal communication, 1993). A large pupillary ruff is visible on the dorsal and ventral margins of the iris.11 This structure is analogous to corpora nigra (iridica) of horses, but consists of vertically folded layers of posterior iridial pigment epithelium rather than globular masses of corpora nigra. These extensive sheets of tissue meet and almost intermesh in very bright sunlight. Their function probably is to shade the pupil, decreasing the amount of light entering the eye. The pupil is roughly oval, with the long axis oriented horizontally. Its lateral and medial portions are smooth and rounded. As in domestic livestock species, pupillary light reflexes are slow.s,11 The fundus of the llama lacks a tapetum, but often appears highly reflective on ophthalmoscopy because of the presence of a prominent, shiny Bruch's membrane that has been identified histologically (Dubielzig RR, personal communication, 1993). The fundus may appear brown because of a pigmented choroid or red because of visibility of choroidal blood vessels through a nonpigmented choroidY The retinal blood vascular pattern is similar to that of caUleY About three pairs of blood vessels emerge from the optic disc. One large pair courses dorsally, the vessels winding around each other. These vessels often appear elevated from the retinal surface. Two pairs course horizontally and often are accompanied by myelinated optic nerve fibers for several disc diameters away from the optic nerve head. Ventrally, either one vessel exits and divides into two, or two vessels exit singlyY The bony orbit of the llama is complete. The orbital rim is made up of a union of the frontal, lacrimal, and zygomatic bones. The maxillary, palatine, temporal, and sphenoid bones also contribute portions to the orbit. A large notch is present in the frontal bone, and may be palpated in the dorsal orbital rimY A large (2-cm) opening communicating with the nasal cavity is present 2 cm rostral to the medial orbit. Its function is unknown, but it may contain a scent glandY
MICROBIOLOGY OF THE CAMELID EYE
Numerous bacteria and fungi species have been cultured from the normal conjunctival sacs of camelidsY-13 In most instances the isolated organisms were similar to those reported from other domestic animal species (Table 2).16,22,25-28 In one study, however, a surprisingly large proportion of llamas, alpacas, and guanacos harbored Pseudomonas.13 None of these isolates was Pseudomonas aerugino sa, (a common cause of melting ulcers in domestic animals), but any Pseudomonas organism may produce disease secondary to ocular trauma. 2 Fungal spores were present in over half the conjunctival sacs of llamas, alpacas, and guanacosY Isolates included Aspergillus and Fusarium, fungi commonly responsible for keratomycosis in domestic animals and humans.9, 10, 17, 18 Although no reports of fungal keratitis or conjunctivitis in camelids are available, the potential for fungal invasion of the cornea is ever present. No other types of conjunctival micro-organisms have been reported isolated from healthy camelid eyes. Although chlamydial organisms were cultured from a llama with conjunctivitis (Severin GA, unpublished data, 1993), to my knowledge no attempts have been made to isolate Chlamydia from healthy eyes. Two studies attempted to isolate Mycoplasma organisms, but none was foundY DISEASES OF THE EYELIDS AND NASOLACRIMAL SYSTEM
Congenital, infectious, and traumatic eyelid diseases occur in camelids. Eyelid lacerations are not common, but can be serious because of possible secondary Table 2. PERCENTAGE OF CAMELIDS POSITIVE FOR BACTERIA AND FUNGI llama Bacteria Gram-positive organisms Coagulase-negative Staphylococcus spp. Coagulase-positive Staphylococcus spp. Bacillusspp. Streptococcus spp. Corynebacterium spp. Streptomyces spp. Gram-negative organisms Pseudomonas spp. Pasteurella spp. Branhamella spp. Moraxella spp. Fungi Aspergillus spp. Fusarium spp. Rhinocladiella spp. Alternaria Mucorspp. Penicillium spp. Curvularia spp.
7 35 22 15 11
6 35 47
14 0.6 0.6 0.6 (n = 109) 33 29 9 7 7 3 3
35 6 29
= 30 4 2
Adapted from Gionfriddo JR, Friedman DS: Ophthalmology of South American camelids: Llamas, alpacas, guanacos, and vicunas. In Howard JL (ed): Current Veterinary Therapy 3: Food Animal Practice. Philadelphia, WB Saunders, 1993, p 842.
corneal damage. All full-thickness lacerations should be sutured. Because camelid eyelids fit tightly on the globe, it is very important to appose the eyelid margins carefully when suturing. Careful apposition prevents secondary entropion and trauma to the cornea from notching or scarring of lid margins. A finegauge absorbable suture material (e.g., 6-0 Vicryl, Ethican Inc, Somerville, NJ) should be used to suture subcutaneous tissue, and a fine nonabsorbable suture (e.g., 4-0 or 5-0 prolene or nylon) should be used in skin. Few congenital eyelid problems are reported in camelids. In llamas they include entropion, trichiasis (Severin GA, unpublished data, 1993), eyelid cysts, ectropion, and eyelid hypogenesis.8 Seidel reported spastic entropion in a llama and described a surgical correction similar to the Hotz-Celsus procedure used in other domestic animals. 24 Blepharitis caused by bacterial infection occurs in llamas (Severin GA, unpublished data, 1993), often in conjunction with bacterial conjunctivitis. Routine culture and sensitivity testing and proper antibiotic therapy have been curative in most blepharitis cases. One blepharitis case was seen in conjunction with a generalized seborrhea-like condition, but the cause of the skin problem was not known (Severin GA, unpublished data, 1993). Nasolacrimal system problems appear to be relatively common in llamas. Congenital punctal atresia was present in four llamas examined at CSU-VTH (Severin GA, unpublished data, 1993). The main sign of punctal atresia is chronic epiphora. Puncta are opened with a procedure similar to th!=lt used in horses. IS Dacryocystitis in llamas, as in most domestic animals, is caused by a foreign body, such as a grass awn, entering through the nasolacrimal punctum. Cannulation of the punctum and flushing of the nasolacrimal sac often is curative. Instillation of antibiotic agents via nasolacrimal cannula often is necessary as well. Keratoconjunctivitis sicca, although known in llamas (Severin GA, unpublished data, 1993) appears to be very rare. No case reports were found describing its occurrence, causes, or treatments in camelids. DISEASES OF THE CONJUNCTIVA
Infectious conjunctivitis and keratoconjunctivitis are diagnosed commonly in llamas. Bacterial infections appear to be most common. Brightman et al4 reported bacterial keratoconjunctivitis in a 3-year-old llama. Clinical signs included blepharospasm, photophobia, and epiphora. Bacterial culture of the inflamed conjunctiva yielded Staphylococcus aureus and the cornea grew Moraxella liquifaciens. Moraxella was considered a pathogen, and proper antibiotic therapy based on sensitivity testing proved curative. Klebsiella pneumoniae, Moraxella spp., Bacteo ides spp., and Streptococcus spp. have been cultured from llamas with conjunctivitis. l l Although suspected to be primary pathogens, that was not demonstrated and several of the organisms could have been secondary invaders. SeideF4 described several cases of purulent and follicular conjunctivitis and catarrhal conjunctivitis in llamas, alpacas, and guanacos in Germany. Symptoms included photophobia, blepharospasm, epiphora, and protrusion of the nictitating membrane. Culture and sensitivity testing were essential in selecting proper antibiotic therapy. Other causes of conjunctivitis apparently are rare in llamas. Chlamydial conjunctivitis was diagnosed in one llama at CSU-VTH (Severin GA, unpublished data, 1993). Parasitic conjunctivitis in llamas has been attributed to both nematodes and flies. Thelazia californiensis is a nematode found in the conjunctival sac of numerous mammalian species, including llamas.8 The parasite is transmitted
from animal to animal by flies. The pathologic effects of this parasite in llamas range from mild conjunctivitiss to severe keratoconjunctivitis and ulcerative keratitis.ll Epiphora is the main presenting clinical sign of infection, and the worm may be seen on the surface of the cornea and conjunctiva, beneath the nictitating membrane, or in the nasolacrimal puncta. s The nematode may be removed mechanically under local anesthesia. Alternatively, diethylcarbamazine or ivermectin drops may be instilled in the conjunctival sac to kill the parasite, which then is flushed from the eye by tears. s Flies often cause an irritant conjunctivitis when they feed on lacrimal secretions of camelids. Fly control is essential to decrease the incidence of this condition. 11 Noninfectious conjunctival diseases include trauma, foreign bodies, and congenital cysts. Eyelid lacerations often are accompanied by tears in the bulbar or palpebral conjunctiva. Large conjunctival wounds should be sutured with small gauge, absorbable suture material. Extreme care should be used to avoid exposing any suture material to the cornea. Conjunctivitis due to foreign material in the conjunctival sac was found in three llamas at CSU-VTH (Severin GA, unpublished data, 1993). The entire conjunctival sac should be inspected carefully for foreign material in all conjunctivitis cases. Schuh et aF3 reported a case of a cystlike structure on the bulbar conjunctiva of one eye of a newborn cria. Aspirations of this structure yielded a clear transudate. Because the same eye had a massive scleral ectasia that extended from an optic disc coloboma to the ventral conjunctiva, the conjunctival cyst structure was considered part of a general ocular maldevelopment. Johnson removed a similar cyst-like structure (Fig. 1) from the bulbar conjunctiva of an otherwise normal eye of a newborn llama (Johnson LW, personal communication, 1993).
Figure 1. Conjunctival cyst in a 24-hour-old cria. Clear fluid was aspirated 24 hours before surgical removal. (Courtesy of LW Johnson.)
DISEASES OF THE CORNEA AND SCLERA
Corneal trauma is one of the more commonly seen ocular problems in llamas. Foreign bodies, lacerations, abscesses, abrasions, and ulcers have been reported.4 ,8,11 Corneal ulcers are quite common and CSU-VTH diagnosed abrasions in two llamas, stromal ulcers in 11 llamas, and perforating ulcers in three llamas (Severin GA, unpublished data, 1993). Ulcerative keratitis in llamas is caused primarily by injury, with secondary invasion of the intact cornea. No known reports of primary bacterial invasion of the intact cornea (as in Moraxella bovis infections in cattle) have been published. Corneal trauma also may be seen in llamas recumbent because of tick paralysis, meningeal worm, or prolonged anesthesia. Treatment of traumatic corneal disease in camelids is similar to that in other species. Because of the presence of potential bacterial pathogens in llama eyes, wounds and ulcers should be treated with topical broad-spectrum antibiotics until culture and sensitivity results are obtained. Lacerations may be sutured directly with fine-gauge suture material. Deep ulcers heal well under the protection of conjunctival pedicle grafts, which are recommended in llamas (Severin GA, personal communication, 1993). Other corneal pathologies seen in camelids include corneal dystrophy/,ll corneal infiltrates, corneal dermoidsp and endothelial degeneration (Severin GA, unpublished data, 1993). Bilateral corneal edema was reported in a female guanaco and its offspring.1 The edema was associated with other ocular defects and probably was due to congenital corneal endothelial dystrophy. Few diseases of the sclera have been reported. Perforating wounds were seen in only two llamas at CSU-VTH (Severin GA, unpublished data, 1993). Extensive protection of the sclera by the tightly-fitting eyelids of llamas may help prevent injury. Episcleral melanomas were seen in two llamas at CSU-VTH (Severin GA, unpublished data, 1993). DISEASES OF THE ANTERIOR SEGMENT: ANTERIOR UVEA AND ANTERIOR CHAMBER
Anterior uveitis seems common in camelids and often occurs in conjunction with chorioretinitis or panophthalmitis. It is characterized by aqueous flare, hyphema, or fibrin in the anterior chamber. As in other domestic species, determining the cause of the uveal inflammation in camelids may be difficult. The cause was unknown in 6 of 11 cases of anterior uveitis at CSU-VTH (Severin GA, unpublished data, 1993). Four of the 11 animals had known traumatic uveitis; one had suppurative uveitis. Anterior uveitis has been observed in septicemic neonates and in llamas with juvenile llama immunodeficiency syndrome (Johnson LW, personal communication, 1993). Anterior uveitis may be secondary to deep ulcerative keratitis in camelids. Uveitis therapy should be instituted in such cases. DISEASES OF THE LENS
Cataracts are the most common abnormalities of the llama lens; 14 of 16 llamas presented to CSU-VTH with lens abnormalities had cataracts (Severin GA, unpublished data, 1993). A large number of llamas undergoing routine ocular examinations at the University of Wisconsin had small, focal cataracts that did
not cause severe visual deficitsY Whether or not such small opacities progress to maturity and cause visual problems is unknown. Many llama cataracts are congenital.1,3, S, 8 Heritability is suspected but has not been demonstrated in llamas in the United States. l l Boer and Schoon3 described cataracts thought to be of autosomal recessive inheritance in vicunas in the Zoological Gardens of Hanover. Some cataracts in camelids impair vision significantly.1,s Attempts to remove cataracts surgically have had limited success.S,14 Many veterinary ophthalmologists reported severe postoperative corneal edema and uveitis after cataract extractions in llamas.u In one case the severe edema progressed to secondary bacterial ulcerative keratitis and eventually to phthisis bulbi,14 A llama that underwent cataract surgery at CSU-VTH had postoperative corneal edema, but some vision was restored (Severin GA, unpublished data, 1993). The causes of severe postoperative corneal edema in llamas after cataract extraction have not been investigated. It has been suggested that llamas may have a highly sensitive corneal endothelium or a high degree of postoperative infiammation,ll which leads to decompensation of the pumping mechanism of the corneal endothelium, allowing fluid to enter the corneal stroma. Because of the apparently low success rate of cataract surgery in llamas and the potential severity of postoperative complications, this surgery is not recommended in general veterinary practice. Other problems reported in the camelid lens include a congenital coloboma in a guanaco/ a traumatic lens rupture in a llama, and a lens subluxation in a llama (Severin GA, unpublished data, 1993). The colobomatous defect was seen temporally in the left lens of a female guanaco, and was associated with nuclear and perinuclear cataracts and corneal edema.1 Corneal edema also appeared in the right eye of this animal but the lens appeared normal. The lack of inflammatory signs and the presence of similar lesions in a female offspring of the guanaco suggested a hereditary cause for the defects. DISEASES OF THE RETINA AND OPTIC NERVE
Congenital and infectious diseases of the retina, choroid, and optic nerve of camelids have been reported. Congenital abnormalities of the posterior segment may be limited to a single structure such as the optic disc or, more often, may involve multiple structures. Dubielzig examined the eyes of three neonatal llamas histologically and found multiple ocular defects, including peripapillary colobomas, vitreous fibrosis and ossification, cataracts, retinal dysplasia, and retinal detachment,u Friedmanl l reported large optic disc colobomas that did not cause any apparent visual deficits in a 10-month-old llama. Schuh et aF3 reported an 8month-old llama with a coloboma measuring 4 mm in diameter, located 4 mm medial and ventral to the optic disc. This was discovered histologically after enucleation. 23 A conjunctival cyst had been seen in the same eye prior to enucleation but could not be seen on histopathology. Ophthalmoscopic examination of the other eye showed a prominent hyaloid arterial remnant and a possible optic disc coloboma. Although colobomas are known to be hereditary in other species of domestic animals,? their heritability has not been established in camelids. Because of the possibility that these ocular problems are hereditary, however, animals with posterior segment defects should not be used in breeding programs. There are numerous anecdotal reports of chorioretinitis and panuveitis in llamas, but an initiating cause was established in very few cases. Fowlerll described several llamas with panuveitis whose ocular problems were preceded by either respiratory or gastrointestinal symptoms. Although severe bacterial pneu-
monias were diagnosed at necropsy, bacteria were not thought to have caused the uveitis. Active chorioretinitis was diagnosed in six llamas at CSU-VTH but no initiating cause was established (Severin GA, unpublished data, 1993). Two of the six llamas had postinflammatory retinal detachments. Two infectious diseases have been shown to cause severe disease of the posterior segment in camelids. The most widely reported is equine herpesvirus 1 (EHV-1). Camelids acquire this infection by contact with equids. Rebhun et aFl reported a group of 21 alpacas and one llama that became blind after exposure to other wild animals (including zebras) at a Florida quarantine station. Four alpacas developed neurologic signs of nystagmus, head tilt, and paralysis. Ophthalmoscopy of the acutely affected animals showed various degrees of vitritis, retinitis, and optic neuritis. Retinal vasculitis, retinal hemorrhages, subretinal exudate, and retinal detachments caused by vitreoretinal traction bands were common. Two alpacas had hypopion and iritis in addition to the posterior segment lesions. Treatments with antibiotics, steroids, vitamins, and diuretics were ineffective, and all affected animals became permanently blind. Ophthalmoscopic examination of animals in chronic stages of disease showed fibroretinal traction bands, posterior lens capsule opacities, and atrophy and darkening of the optic disc. The diagnosis of EHV-1 was suspected when eosinophilic inclusion bodies were seen in brain sections of the dead alpacas, and was confirmed by serology. A similar outbreak of EHV-1 occurred in Illinois in 1989, when 17 of 28 llamas exposed to zebras with rhinitis developed blindness, deafness, head tilt, and circlingP Ophthalmoscopy showed severe chorioretinitis with sub retinal exudates and hemorrhage, and retinal detachments. Concurrent anterior uveitis was present in most of the animals. EHV-1 was confirmed by observation of numerous intranuclear inclusion bodies in the brains and retinas of the llamas, and by virus isolation from brain tissue of two llamas and the buffy coat from the blood of one zebra. Ocular inflammation was resolved in most llamas, although six animals remained blind. Paulsen et aP9 reported the case of a 5-year-old llama with chorioretinitis, optic neuritis, and encephalitis probably due to an infectious cause. Clinical signs consisted only of blindness and loss of pupillary light reflexes. Ophthalmoscopy showed attenuated retinal blood vessels, pale optic discs, and retinal scars. Histopathologic lesions suggested an infectious cause, but eosinophilic inclusion bodies could not be demonstrated in the brain. Although serologic tests failed to implicate a viral cause, viruses could not be ruled out. Analysis of paired serum samples, which may have better identified a significant viral titer, was not performed. The similarity to the chronically affected alpacas described by Rebhun21 suggests this may have been an instance of chronic EHV-1 infection in which the organism was difficult to isolate. Another confirmed infectious cause of chorioretinitis in camelids is aspergillosis. A young female alpaca, new to the Milwaukee County Zoo, had signs of blindness, head tilt, and circling.20 Ocular examination showed dilated pupils, absence of pupillary light reflexes, pale areas of retinal elevation in the tapetal and nontapetal regions of the fundus, retinal hemorrhages, and optic neuritis. Despite therapy, the alpaca's condition worsened and she became anorexic and died. Necropsy demonstrated disseminated aspergillosis that was thought to have spread to the eye hematogenously. Toxoplasmosis, a known cause of chorioretinitis in dogs and cats, also may lead to blindness in llamas. During an investigation of causes of late-term abortions in llamas, a serologic survey of affected versus normal females uncovered an extremely high titer for Toxoplasma in a nonaborting blind llama. The llama
had been blind for over 5 years and had lesions of chronic panophthalmitis, including anterior synechiae (Johnson LW, personal communication, 1993). Noninfectious causes of blindness also have been demonstrated in camelids. Retinal detachment was diagnosed in four llamas at CSU-VTH (Severin GA, unpublished data, 1993). Two of these were known to be caused by trauma and two others appeared to be spontaneous. As in other species of domestic animals, diseases of the vitreous in camelids usually are secondary to chorioretinitis. In the EHV-1 cases previously described, vitritis was prominent. Of four cases of camelid vitreal disease treated at CSUVTH, three were cases of vitreal exudate and hemorrhage associated with chorioretinitis of unknown origin (Severin GA, unpublished data, 1993). The other was a llama with asteroid hyalosis, a degenerative change of the vitreous. The only reported primary vitreal problems are aging and congenital abnormalities such as vitreal fibrous ossification (usually in conjunction with multiple posterior segment defects). MISCELLANEOUS DISEASES
Congenital visual deficits are being diagnosed with increasing frequency in camelids. From 1980 to 1992, 11 blind neonatal crias with ophthalmoscopically normal fundi were seen at CSU-VTH (see Table 1). In all cases, vision returned gradually, but no cause was found. Congenital nystagmus and amblyopia also have been diagnosed in young llamas (see Table 1). Glaucoma apparently is rare in camelids and no reports of uveitis or panophthalmitis mentioned glaucoma as a secondary complication. Glaucoma was found in normal-appearing eyes of two llamas at CSU-VTH (Severin GA, unpublished data, 1993). Barrie et all used gonioscopy to examine a guanaco with corneal edema and found the iridocorneal angle closed and spanned by uveal tissue from the 2 o'clock to the 4 o'clock positions. The incidence of goniodysgenesis and consequent glaucoma in camelids is unknown. Routine tonometric measurements and gonioscopy on diseased and healthy eyes may reveal a higher incidence of glaucoma than has been reported. Trauma to the orbit and globe has been reported (Severin GA, unpublished data, 1993). Orbital infection, ocular prolapse, and ruptured globes are consequences of severe facial injury. Enucleation often is the only method of dealing with these problems. SUMMARY
Review of the limited literature on camelid eyes suggests they are anatomically similar to those of domestic livestock species, except they lack meibomian glands and have iridial folds (rather than corpora nigra). The microbial flora of the healthy camelid conjunctival sac also appears to be similar to those of domestic livestock and pets, except that no Mycoplasma have been isolated from camelids. Ocular diseases for which camelids are presented to veterinarians are numerous and varied. The most frequently presented conditions are ocular trauma and congenital abnormalities. Trauma to cornea, conjunctiva, eyelids, and sclera has been reported. Therapies for these injuries are the same as for other animals. Most congenital abnormalities are cataracts and optic nerve colobomas, but congenital eyelid defects, conjunctival cysts, and multiple ocular defects have been reported. Although these conditions are not demonstrably hereditary, breeding of animals with congenital ocular defects is strongly discouraged.
Intraocular inflammatory diseases are seen commonly in camelids. Uveitis and chorioretinitis may cause permanent visual loss, usually with no indication of cause. Equine herpesvirus 1 has been isolated from camelids with severe ocular inflammation and is a known cause of chorioretinitis and neurologic abnormalities. Systemic aspergillosis causes severe chorioretinitis in alpacas. More research is needed to improve our understanding of ocular physiology and pathology in camelids. Genetic studies also are needed to establish hereditary patterns of ocular maldevelopment. Additional information from researchers and practitioners should improve our ability to recognize and treat ocular disease in camelids.
References 1. Barrie KP, Jacobson E, Peiffer RL: Unilateral cataract with lens coloboma and bilateral corneal edema in a guanaco. J Am Vet Med Assoc 173:1251-1252, 1978 2. Bistner SI, Roberts SR, Anderson RP: Conjunctival bacteria: Clinical appearances can be deceiving. Mod Vet Pract Dec 50:45-47,1969 3. Boer M, Schoon HA: Untersuchungen zu erblich bedingten Augen-und ZN5-Verdanderungen in einer Zuchtgruppe von Vikunjas (Lama vicugna) im Zoologischen Garten Hanover. Verhandlungsbericht-des-Internationalen-Symposiums-uber-die-Erkankungen-der-Zootier 26:159-164, 1984 4. Brightman AH, McLaughlin SA, Brumley V: Keratoconjunctivitis in a llama. Vet Med Small Anim Clin 76:1776-1777, 1981 5. Donaldson LL, Holland M, Koch SA: Atracurium as an adjunct to halothane-oxygen anesthesia in a llama undergoing intraocular surgery. Vet Surg 21:76-79, 1992 6. Duke Elder S: System of Ophthalmology, vol. 1. The Eye in Evolution. St Louis, CV Mosby, 1958, P 458 7. Falco M, Barnett KC: The inheritance of ocular colobomata in Charolais cattle. Vet Rec 102:102-104, 1978 8. Fowler ME: Medicine and Surgery of South American Camelids. Ames, Iowa State University Press, 1989, p 391 9. Francois J: Les Mycoses Ocularis. Paris, Masson and Cie, 1968, p 134 10. Gerding PA, McLaughlin SA, Troop MW: Pathogenic bacteria and fungi associated with external ocular diseases in dogs: 131 cases (1981-1986). J Am Vet Med Assoc 93:242-244, 1988 11. Gionfriddo JR, Friedman DS: Ophthalmology of South American camelids: Llamas, alpacas, guanacos and vicunas. In Howard JL (ed): Current Veterinary Therapy 3: Food Animal Practice. Philadelphia, WB Saunders, 1993, p 842 12. Gionfriddo JR, Gabal MA, Betts DM: Fungal flora of the healthy camelid conjunctiva] sac. Am J Vet Res 53:643-645, 1992 13. Gionfriddo JR, Rosenbusch R, Kinyon JM, et al.: The bacterial and mycoplasmal flora of the normal eye of captive camelids. Am J Vet Res 52:1061-1064, 1991 14. Ingram KA, Sigler RL: Cataract removal in a young llama. In Proceedings of the 1983 Annual Meeting of the American Association of Zoo Veterinarians, Tampa, FL, 1983 15. Lavach JD: Large Animal Ophthalmology. St Louis, CV Mosby, 1990, P 394 16. Lundvall RL: The bacterial and mycotic flora of the normal conjunctival sac in the horse. Proc Am Assoc Equine Pract: 101-107, 1967 17. Mitchell JS, Attleberger MH: Fusarium keratomycosis in the horse. Vet Med Small Anim Clin 1257-1273, 1973 18. Moore CP, Fales WH, Whittington P, et al: Bacterial and fungal isolates from Equidae with ulcerative keratitis. J Am Vet Med Assoc 182:600-603, 1983 19. Paulsen ME, Young S, Smith JA, et al: Bilateral chorioretinitis, centripetal optic neuritis, and encephalitis in a llama. J Am Vet Med Assoc 194:1305-1308, 1989 20. Pickett JP, Moore CP, Beehler BA, et al: Bilateral chorioretinitis secondary to disseminated aspergillosis in an alpaca. J Am Vet Med Assoc 187:1241-1243, 1985
21. Rebhun WC, Jenkins DH, Riis RC, et al: An epizootic of blindness and encephalitis associated with a herpesvirus indistinguishable from equine herpesvirus 1 in a herd of alpacas and llamas. J Am Vet Med Assoc 192:953-956, 1988 22. Samuelson DA, Andersen TL, Gwin RM: Conjunctival fungal flora in horses, cattle, dogs, and cats. J Am Vet Med Assoc 184:1240-1242, 1984 23. Schuh JCL, Ferguson JG, Fisher MA: Congenital coloboma in a llama. Can Vet J 32:432433, 1991 24. Seidel B: Augenkrankheiten bei Neuweltkemelen. Erkrankungen der Zootiere. Verhandlungssbericht des 31. Intemationalen Symposiums uber die Erkrankungel1, der Zoound Wildtiere, Dortmund 1989, pp 79-82 25. Spadbrow P: The bacterial flora of the ovine conjunctival sac. Aust Vet J 44:117-119, 1968 26. Urban M, Wyman M, Rheins M, et al: Conjunctival flora of clinically normal dogs. J Am Vet Med Assoc 161:201-206, 1972 27. Whitley RD, Burgess Ee, Moore CP: Microbial isolates of the normal equine eye. Equine Vet J 15(suppI2):138-140, 1983 28. Wilcox GE: Bacterial flora of the bovine eye with special reference to the Moraxella and Neisseria. Aust Vet J 46:253-257, 1970
Address reprint requests to Juliet R. Gionfriddo, DVM, MS Eye Clinic for Animals 10333 Metcalf Avenue Overland Park, KS 66212