Ocular biology and diseases of Old World chameleons

Ocular biology and diseasesof Old World chameleons

Rob L. Coke, DVM*, Natassia K. Couillard, DVMExotic Animal, Wildlife, and Zoo Animal Medicine Service,

Department of Clinical Sciences, College of Veterinary Medicine,

Kansas State University, Manhattan, KS 66506, USA

Biology

Function in prey acquisition

To capture insects, chameleons scan their environment by moving their

eyes independently in saccadic movements (Fig. 1). These rapid, jump-like

movements are more frequent and larger in size than those of other animals

and promote gaze stabilization [1]. The chameleon eye can move 180� in the

horizontal plane and 80� in the vertical plane, which requires intricate coor-

dination between the extraocular muscles of the eye and the motorneurons

that supply them [2].

As they locate a potential prey insect, chameleons visually fixate andalign their head with the prey. In the protrusion phase, the chameleon opens

its mouth slightly and extends its tongue slightly beyond its mouth. The cha-

meleon determines its distance from the target by direct accommodation

and uses one eye to target and measure distance to the prey item [3].

Before tongue projection, both eyes fixate toward the target. Earlier lit-

erature believed the eyes became fixed within the head during this process

[4,5]. With the lack of convergent eye movements, the retinal prey image

becomes depicted extrafovally if the distance to the prey is changed. Theextrafoval movements create a large field of motion to allow the chameleon

to simultaneously track two different objects and to allow foveal pursuit and

tracking movements for single objects [3,5]. As the head tracks the prey in

preparation for the tongue shoot, the angle between the head and the eye

is divergent at approximately 17� to 19�. This angle is fixed despite changes

in distance from the target [5].

* Corresponding author. Oklahoma City Zoo, 2101 NE 50th Street, Oklahoma City,

OK 73111, USA.

E-mail address: [email protected] (R.L. Coke).

1094-9194/02/$ - see front matter � 2002, Elsevier Science (USA). All rights reserved.

PII: S 1 0 9 4 - 9 1 9 4 ( 0 1 ) 0 0 0 0 7 - X

Vet Clin Exot Anim 5 (2002) 275–285

The hyoid apparatus extends in the projection phase and places full ten-sion on the tongue, which is projected out to the target up to 5 m/s [3]. The

length of the tongue projection is directly proportional to the prey-target

distance derived from accommodation [6].

Cornea

The cornea has a considerable role in overall optic power and in accom-

modation, whereas the lens has a small role. This principle enables the cha-

meleon to rapidly locate its prey and discern it from the background [7].

Nasolacrimal duct

The conjunctival opening of the nasolacrimal duct is located away from

the eyelid opening near the fornix at about 8 o’clock (left side) or 4 o’clock

(right side) around the orbital rim. The duct runs from the opening, through

a bony channel inside the maxilla, and out to the nares with an internal

opening to the inner choana.

Lens

The lens of the chameleon is slightly biconvex and has a negative refrac-

tive power when unaccommodated, as compared with that in other verte-

brates with positively powered lenses. As light passes through the lens, it

diverges to create a larger image on the retina. This occurs because the lens

Fig. 1. Veiled chameleon (Chamaeleo calyptratus). The eyelids are fused to form a small

opening around the glob. The eyes are independent and highly mobile.

276 R.L. Coke, N.K. Couillard / Vet Clin Exot Anim 5 (2002) 275–285

is powered negatively and is biconvex with peripheral lens pads consisting of

a high index material. The negative lens creates a larger accommoda-

tion range. The cornea is a positive-powered optic positioned anterior to

the negatively powered lens. This setup creates an optical system in whichthe focal length is greater than the actual length, increasing magnification

to enable chameleons to precisely focus on prey objects. This process is anal-

ogous to a photographer’s telephoto lens; after focusing, the distance to the

target can be read off of the focus ring on the camera lens [8,9].

In other vertebrates, the evolutionary trend is to increase corneal power

and decrease lens power to aid in visual acuity. Chameleons use this

mechanism to the exclusion of any other method and are extremely accu-

rate. Mammals with binocular vision use other techniques, such as triangu-lation, to approximate the distance to the target [8]. Before tongue

projection, chameleons use eyes when accommodating a target, but they

do not triangulate between their eyes and the target. The angle of conver-

gence between the eyes is too variable to allow triangulation or stereopsis.

This coupled accommodation with both eyes allows for an increased preci-

sion of distance measurement [3].

Retina

The outer layers of the retina in the chameleon differ from that in other

vertebrates by several anatomic factors. The inner nuclear layer contains

three types of neurons: GABA(c-aminobutyric acid)nergic amacrine cells(90%), displaced ganglion cells, and interplexiform cells. There are two types

of interplexiform cells: type I cells are located centrally and peripherally, and

type II cells are only found in the periphery [10].

At the visual streak, a high density of ganglion cells enhances the chame-

leon’s visual system. This ganglion cell distribution is believed to aid in

visual acuity and detection of movement [11].

Only cones are found in the chameleon retina, and two types are de-

scribed: single and double cones. Yellow-green oil droplets, which are roundto oval and sometimes pyriform in shape, are located within both types

[12]. These droplets are highly refractive and function to collect light [13].

Because chameleons are diurnal, the areal density of cones is large.

There are two zones in the outer nuclear layer. One zone includes the cen-

tral retina, fovea, and parafovea. Cones are distributed throughout the layers,

and the axons terminate in small pedicles. The other zone is the periphery in

which cones are arranged in a single layer and axons end in a pedicle that is

larger than that in the other zone [14].

Brain and optic tectum

Visual information is transmitted along the axons of the ganglion cells,

which exit from the caudal aspect of the retina and join to form the opticchiasm at the diencephalon. Here, the optic fibers completely decussate, and

277R.L. Coke, N.K. Couillard / Vet Clin Exot Anim 5 (2002) 275–285

there is no ipsilateral projection of these axons. Contralaterally, they

converge to form the marginal optic tracts (MOTs) that terminate at the

primary visual center [15]. Unlike other vertebrates, chameleons have ahighly developed optic system in which a number of secondary interconnec-

tions between the optic tectum and nuclei in the diencephalon and midbrain

enhances the optical response to visual stimuli. The exact function of the

nucleus opticus tegmenti is unknown but is believed to control eye move-

ments. It has direct connections with the oculomotor nucleus and has some

indirect connections to the aduceus and trochlear nuclei [16].

Ocular examination

A detailed and thorough history is invaluable in determining potential

disease in chameleons. Each owner should complete a detailed history formcontaining questions on the caging, environment, and previous medical his-

tory, including the types of food (eg, crickets, superworms, waxworms), and

the percentages of each eaten item.

A thorough, systematic approach to the examination provides clues to an

appropriate diagnosis. Chameleons have sharp claws, and the large species

have a noticeable bite. The patient should be examined as it climbs on a

perch for general demeanor, and it should be restrained for the rest of the

examination by grasping the base of the head behind the eyes by the thumband forefinger. This approach allows complete control of the head. The

palm of the hand should rest along the back, allowing fingers to catch the

chameleon’s feet.

Enophthalmia is a common indicator of disease. It usually is combined

with other signs such as anorexia, dehydration, and emaciation. Sunken eyes

are generally a poor prognostic indicator. Exophthalmia is another common

sign of disease. Swelling can come from the globe itself, the surrounding

conjunctiva, or the retrobulbar space [17–19].

Diseases

Noninfectious diseases

Corneal damage can come from trauma secondary to shipping or aggres-

sion. Superficial lesions are responsive to typical treatments with common

ophthalmic antibiotic preparations. Deep corneal lesions or lacerations may

require enucleation if medical therapy is unsuccessful or if they involve the

aqueous chamber.

Periocular swelling (Fig. 2) does not have a defined cause but can result

from husbandry-related issues such as contact irritants, vitamin A defi-ciency, decreased ventilation or humidity, and foreign bodies. One case of

periocular swelling in a dwarf chameleon was reported from a bee sting. The


resultant swelling systemically did not affect the chameleon, and the eye

returned back to normal size [20].

Certain tropical plants (Ficus, Pothos spp) often are used in chameleon

enclosures and have been associated with conjunctivitis. These plants con-

tain oxalates within the leaves and as white residue on the leaf surface. This

excess residue may come in contact with the eye and cause conjunctivitis.

Though these plants are used routinely in chameleon enclosures, it is impor-tant to keep them misted several times a day to prevent the build up of

excess oxalates. Chameleons that are housed in glass aquaria have an

increased risk for ocular disease because of decreased ventilation. Changing

the enclosure to a wire mesh cage often can be beneficial.

Vitamin A deficiency commonly is associated with ocular abscesses and

matted eyes but also is linked to reproductive and neonatal disorders in cha-

meleons [17,21]. During a study by Ferguson, the affects of vitamin A and D

were evaluated with reference to exposure to ultraviolet (UV) A and B.Compared with chameleons exposed to high levels of vitamin A, chameleons

exposed to low levels of vitamin A had an increased incidence of tail-tip

necrosis, swollen lips, gular or cervical edema, vertebral abnormalities, hemi-

penal impaction (males), and eyelid closure and ocular discharge. The ocular

signs were associated with anorexia and rapid debilitation [21]. The resul-

tant squamous metaplasia from vitamin A deficiency can lead to xeroph-

thalmia and build up of desquamated cells. Material collects in the

large conjunctival sac of the chameleon and blocks the nasolacrimal duct,compounding the disease process and resulting in further conjunctivitis [22].

Fig. 2. Jackson’s chameleon (Chamaeleo jacksoni) with periocular swelling that is associated

with orbital absecessation.


Foreign bodies such as dirt, sand, or dust may enter the small eyelid open-

ing and become trapped in the deep conjunctival sacs. The conjunctival fornix

is located around 180�, forming a vertical hemisphere. In nature, chameleonscorrect the problem by drinking excessive water during rain showers. The

water is flushed from the oral cavity, up the choana, through the nasolacrimal

duct, and out into the conjunctival sac. The eyes greatly bulge outward and

rotate, allowing the water to flush the conjunctival sac. In captivity, this pro-

cess can be simulated by placing the chameleon in the shower, outside under

an artificial sprinkler system, or outside during a light rain.

Noninfectious diseases of the musculosketetal system are common in cha-

meleons. Metabolic bone disease (MBD) is one of the most common mus-culosketetal diseases seen in clinical practice. It is a multifactorial disease

of calcium metabolism. Clinical signs include lethargy, multiple fractures,

deformed or curled limbs, rubber jaw, and stunted growth. This syndrome

in chameleons resembles the secondary nutritional hyperparathyroidism and

fibrous osteodystrophy commonly seen in the green iguana (Iguana iguana).

If the bones around the orbit are affected, the swelling may affect ocular

movement and partially prolapse the eye. If the bone surrounding the naso-

lacrimal duct is affected, the resulting occlusion may predispose the conjunc-tival sac to secondary swelling and infection. The major contributing factors

of MBD include insufficient dietary calcium intake, lack of available UVB

light, insufficient vitamin D3, and excess of dietary phosphorus. Treatment

of this form of MBD follows the same guidelines established for other lizard

species. The goal of treatment is to establish a positive calcium balance by

proper supplementation of calcium and adequate exposure to UVB light

[19,23,24].

Neoplasia of the eye and surrounding adnexae has not been documentedoften in reptiles. Several cases have been linked to viral causes such as papil-

lomas in green lizards (Lacerta sp), poxvirus in spectacled caimans (Caiman

crocodilus), and a herpesvirus in green sea turtles (Chelonia mydas) [22].

Squamous cell carcinomas have been associated with the skin of the head

and eyelids in other reptiles, with one study listing Jackson’s chameleon

(Chamaeleo jacksoni) as an example [25].

Infectious diseases

Periocular swelling can come from the globe itself or the surrounding tis-

sues. The globe can increase in size because of uveitis, panophthalmitis, or

glaucoma. Swelling from the surrounding tissues may stem from conjuncti-

vitis, retrobulbar abscesses, orbital osteomyelitis, or parasitic infection. An

infection can come from the conjunctiva proper or as an ascending stoma-

titis from the nasolacrimal duct [26]. Treatment with systemic antibiotics

(Table 1) provides better antibiotic levels in the intraocular and subcuta-neous tissues than does topical treatment alone. In severe abscesses, surgical

debridement may prove beneficial [27]. If the eye causes discomfort


(ie, cage rubbing or clawing is observed), an ophthalmic nonsteroidal

anti-inflammatory such as flurbiprofen (Ocufen, Allergan Medical Optics:

Irving, CA) can be applied one to two times daily.

Osteomyelitis around the orbit can be a devastating disease in chame-

leons. Aggressive therapy is needed for these cases. Initial treatment consists

of aggressive surgical debridement and deep antiseptic wound cleansing. Forbacterial infections, a culture and sensitivity are valuable in antibiotic selec-

tion. Treatment with appropriate antibiotics based on sensitivity generally

lasts for a minimum of 8 to 12 weeks and can extend to 6 months. Even with

appropriate treatment, prognosis is generally poor.

Parasites with migrating larval stages sometimes invade the conjunctival

tissues, retrobulbar tissues, intraocular space, or the conjunctival sac. Hex-

ametra angusticaecoides is an intestinal nematode with an extensive larval

migration with direct and indirect life cycles [28]. Malagasy chameleons arethe definitive hosts but may serve as intermediate hosts [29,30]. In one report

of an infection of a veiled chameleon (Chamaeleo calyptratus), larvae were

widespread in the liver, coelomic cavity, subcutaneous skin, and retrobulbar

space [31]. Foleyella furcata and F. brevicauda are filariid worms that have an

extensive migration pattern. They have a 6-month interval between time of

infection and production of microfilaria in the bloodstream. An Oustlet’s

chameleon (Chamaeleo oustaleti) was reported to have Foleyella sp in a fluc-

tuant swelling of an upper eyelid [32]. Other reports of Foleyella sp in chame-leons found that these parasites may be located in the coelomic cavity and

muscles [33]. Surgical removal of the parasites may provide relief and return

to normal visual function. Typical parasiticides may not remove these para-

sites completely and may cause toxic reactions from the decaying parasites.

The black snake mite (Ophionyssus natricis) and red chigger mites (Trom-

biculidae) are seen infrequently in chameleons. Treatment is challenging.

The key to treatment lies in complete environmental sanitation. Ivermec-

tin can be used to eliminate the mites. Care must be taken with ivermectin

Table 1

Systemic antimicrobial formulary for Old World chameleons

Drug Dose (mg/kg) Frequency Route

Amikacin 2.5–5 Every 24–72 h IM

Azithromycin 10 Every 24–48 h PO

Ceftazidime 20 Every 24–48 h IM

Clindamycin 5 Every 24 h PO

Enrofloxacin 5–10 Every 24 h PO, IM, SC

Metronidazole 20–50 Every 24–48 h PO

Piperacillin 100–200 Every 24 h IM

IM¼ intramuscularly; PO¼orally; SC¼ subcutaneously. Data from Carpenter JW,

Mashima TY, Rupiper DJ. Exotic animal formulary. 2nd edition. Philadelphia: WB Saunders;

2001. p. 41–105; and Plumb DC. Veterinary drug hand book. 3rd edition. Ames: Iowa State

University; 1999. p. 853.


treatment because of several antedotal reports of adverse reactions in chame-

leons [17]. Soaking chameleons is not accomplished easily; topical products

tend to be easier to apply and are more effective. Fipronil (Frontline,Rhone-Merieux, Athens, GA), which is labeled only for use in dogs and cats

for the topical treatment of fleas and ticks, is effective against mites and is

applied topically. Potential side effects in reptiles have not been investigated,

and use of this drug in reptiles is considered extra-label. When combined with

proper environmental sanitation, one to two applications 2 weeks apart

seems to eliminate the mites.

Therapeutics

An ocular and nasolacrimal flush may be beneficial in cases of conjunc-tivitis and removes dirt and other foreign material that may be trapped

in the conjunctival space. An ophthalmic irrigation solution (AK-Rinse,

Akorn, Buffalo Grove, IL)1 can be used with a soft-tip rubber catheter, a

blunt-tip nasolacrimal cannula, or a small-tip metal feeding tube. The can-

nula or catheter is placed inside the eyelid opening and directed away from

the cornea. Application of gentle pressure on the syringe allows flushing of

the conjunctival sac, and the excess fluid exits the eyelid opening. Alterna-

tively, the eyelids can be closed around the tube to allow flushing throughthe nasolacrimal duct. The chameleon should be positioned in with its head

down to allow excess fluid to drain out of the mouth to prevent aspiration.

The fluid that passes through the nasolacrimal duct and choanae can be col-

lected and prepared for cytologic analysis. Aerobic culture and sensitivity

are indicated if the cytology suggests an inflammatory reaction. An ophthal-

mic antibiotic preparation (Table 2) can be used as a flushing agent to treat

the bacterial infection [34].

1 At this time, no drugs have been approved or completely studied in chameleons. All drugs

and doses in this article and both tables are empirical and are derived from other sources and

experiences.

Table 2

Ophthalmic drug formulary for Old World chameleonsa

Drug Dose Frequency

Bacitracin/neomycin/polymyxin B sulfate ointment Small amount Every 12–24 h

Chloramphenicol ointment (1%) Small amount Every 12–24 h

Ciprofloxacin drops (3 mg/mL) 1 drop Every 12–24 h

Gentamicin drops (3 mg/mL) 1 drop Every 12–24 h

Gentamicin ointment (3 mg/g) Small amount Every 12–24 h

Oxytetracycline/polymyxin B sulfate ointment Small amount Every 12–24 h

Tetracycline HCL Ointment (10 mg/g) Small amount Every 12–24 h

Flurbiprofen sodium drops (0.03%) 1 drop Every 12–24 h

a Ophthalmic ointments can be applied using a sterile cotton-tip swab to aid in application.


Because of the visual impairment (even with mild disease), the chameleon

is often anorexic, and supportive care (including syringe feeding or hand

feeding) may be needed. The ocular and nasolacrimal flush is a useful

adjunct in treating periocular swelling; it prevents ocular or orbital damageand is a nonsurgical means of removing foreign debris from the conjunctival

space and clearing the nasolacrimal duct [34].

Once conjunctivitis begins, aggressive treatment also must begin. In many

cases, the chameleon should be sedated or anesthetized to facilitate treat-

ment. The anesthetic protocols for chameleons are similar to those of other

reptile species. Injectable anesthetics in chameleons include ketamine (20–30

mg/kg IM) or preferably propofol (Rapinovet, Mallinckrodt, Mundelein,

IL). Propofol rapidly induces anesthesia and has short recovery times, withdoses ranging from 5 to 10 mg/kg IV in the ventral tail vein or interosseously

(IO) in the femur [35–37]. This dose provides a rapid induction, with dura-

tions of surgical anesthesia of 10 to 25 minutes. The chameleon is usually

ambulating and recovering 25 to 40 minutes after the injection. For longer

procedures, propofol can be used as an induction agent for gas anesthesia at

5 mg/kg IV or IO. Isoflurane (Isoflo, Abbott, Mendota Heights, MN) is the

gas anesthetic of choice for most lengthy surgical procedures. If an inject-

able induction agent is not used, chameleons can be induced with a smallcone mask or a converted syringe case mask. The induction starts at 1%

to 2%, gradually moving up to 4% to 5%. Once an appropriate depth of

anesthesia is attained, the isoflurane is maintained at 1% to 3% for the dura-

tion of the procedure [18].

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Ocular biology and diseases of Old World chameleons