1. Abstract

Since ocular lesions in birds are an expression of systemic disorders more than in mammals, they represent an important diagnostic criterion. The ocular symptomatology frequently enables specific conclusions to be drawn on suspected disorders or it may even be pathognomonic for a certain disease. Thus, the avian eye may be seen-in a much larger extent than in mammals-as a "diagnostic window." On an average, up to 35 % of all traumatized birds (incidence generally higher in raptors than in pet birds) are suffering from ocular lesions, which are most often hidden within the inner structures of the eye. Ophthalmoscopy, i.e., examination of the posterior eye segment, therefore is obligatory in traumatized birds. Regarding to these facts avian ophthalmology is not a highly specific working field within avian medicine but it should be an integral part of the general examination procedure.

2. Significance of visual capacities

Visual function in birds is essential for flying, surviving in the wild and reproduction. The eye as the main sense organ in birds and its visual capacities have no general superiority compared to mammals but shows a highly specialization as an adaptation to living conditions. Thus visual acuity is 2 to 8 times higher compared to mammals, visual fields are up to 360°, stereopsis ranges from 0° to 70°, maximum spatial frequency (the ability to resolve a certain movement into single frames) is up to 160 frames/sec (10-15 in man) and minimum detection of movements is up to 15°/hour (very slow movements). It should be recognized that ultraviolet-perception (UV-perception between 320 and 680 nm), an ability common in diurnal birds bound to special UV-sensitive rods within the retina and an aspect not investigated very well to date, plays a probably plays a very important role in inter- and intraspecific communication based on plumage-UV-reflection, even in birds which appear monomorphic for the human eye, for the identification/assessment of fruit ripeness based on varying UV-reflection of fruit wax layers, for phenomena of camouflage, orientation other. On the other hand, even complete blindness is not a reason for euthanasia in pet birds. Thus, canaries, suffering from blindness due to cataract formation-a condition which occurs quite often in this species-act normal, as long birds as long as the interior of the cage or aviary is not modified.

3. Anatomical peculiarities

Though there exist numerous anatomical and physiological difference-like the striated rather than smooth intraocular musculature, the anangiotic fundus oculi, the pecten oculi-basically the approach to avian ophthalmology is quite similar to that employed in mammalian ophthalmology. Some anatomical peculiarities with relevance for the ophthalmologist are:

1.  Size and weight of the avian eye

a.  Axial length 8 mm (Kiwi, Aptery sp.) up to 50 mm (Ostrich, Struthio camelus).

b.  Weight (Oculus sinister (OS) and oculus dexter (OD) in man 1 %, Fowl 7 % (adult) resp. 12 % (juv.) compared to overall head weight.

2.  Shape

a.  Determination by anulus ossicularis sclerae (10-10 single bony platelets) .

b.  Flat type (diurnal birds with narrow heads, for example columbifomes).

c.  Conical type (diurnal birds with broad heads, for example falconiformes).

d.  Tubular type (nocturnal birds, for example strigiformes).

3.  Adnexal structures

a.  Eyelids

i.  Palpebra inferior larger than palpebra superior (exclusive owls).

ii.  Lower eyelid with "tarsus," no meibomian glands.

iii.  Membrana nictitans highly motile, regulation of praecorneal tear film, protective function for cornea, "snorkel mask effect" (compensation for loss of refractive power during underwater vision).

b.  Lacrimal glands

i.  Small or absent glandulae lacrimaliae.

ii.  Large glandula lacrimalis membranae nictitantis (vel. Harderian gland).

iii.  Replacement by nasal salt gland (aquatic species).

c.  No musculus retractor bulbi

d.  Complete decussation of chiasma opticus (no consensual pupillary reflex)

4.  Anterior eye segment

a.  Striated intraocular musculature (highly motile iris corresponding to external stimuli, no sensitivity to parasympatholytics/sympathomimetics, no reliable pupillary reflex corresponding to light stimuli).

b.  Fundus diameter much larger than pupil diameter .

c.  Ligamentum pectinatum/ciliary cleft with species specific peculiarities.

d.  Lens with anulus pulvinus ("Ringwulst"), accommodation range 2 (owls) up to 80 (waterfowl) D.

5.  Posterior eye segment

a.  Avascular (anangiotic) retina.

b.  Afoveate, uni- or bifoveate retina.

c.  Rods and cones (inclusive special UV-cones) in functional units.

d.  UV-sensitive cones in most diurnal birds.

e.  Slight retinal pigmentation in nocturnal, heavily pigmented retina in diurnal birds.

f.  No retinal tapetum lucidum.

g.  Pecten oculi.

h.  Choroidal, heavily pigmented structure.

i.  Protruding into the vitreous.

j.  Obscuring papilla nervi optici.

k.  Pleated, vaned and conical type.

l.  32 functional theories: nutritive, thermo- and pressoregulative function most obviously.

4. Ophthalmologic equipment and examination procedures in birds

Minimum requirement for basic and general purposes:

 Focused light source with magnification lens (Finoff transilluminator).

 Instrumentation for manipulation of the eye lids (Graefe hook).

 Lacrimal cannula (Anel) .

 Topical anesthetics: Proxametacain, Oxybuprocain (duration of action approx. 7-8 min.) or Lidocaine (duration of action approx. 17 minutes, 12).

Routine equipment

 Slit lamp (magnification x 5-x 15, better x 20)

 Monocular direct ophthalmoscope with 15 D lens or even better.

 Head band ophthalmoscope with 30 and 78 D lens (additional aspherical 40, 60, 90 D).

General examination procedure-Adnexal structures and anterior eye segment

 Without restraint:

 Assessment of visus via food intake, reluctance to fly, orientation.

 With restraint:

 Examination of the ear opening.

 Pupillary reflex.

 Examination of the anterior eye chamber with lateral illumination.

 Examination of the anterior eye chamber with lateral transillumination.

 Examination of the anterior eye chamber with retroillumination.

Equipment and procedure for specific examinations

 Slit lamp biomicrography.

 Gonioscopy (Lovac lens), examination of the angulus iridocornealis with the pectinate ligamentum. Etiological assessment of primary/secondary glaucoma status.

 Tonometry. Estimation of the intraocular pressure (IOP). Use electronic short time acting tonometer or Schioetz-Tonometer in raptors. Standard reference values measured with an electronic tonometer calibrated for avian eyes, range from 9 to 22 mg Hg and are available for 42 species from 7 orders. Minimum corneal diameter for reliable value is 9 mm.

 Schirmer-Tear-Test or better Phenol-red-thread-test (PRT). Test for the estimation of the lacrimal function. Use standardized filter strips of 2, 3 and 5 mm width. Standard reference values using filter strips of various width for 42 species from 7 orders showing a wide range of interspecies variations are available. Strigiformes show conspicuously low values.

 Electroretinography. Measurement of retinal function by recording electrical potentials after light stimulation. This technique gives no information about the visus, only on retinal function. Basic principles of electroretinography for routine examination have been established. Indications are retinal disorders and diotric apparatus opacities.

 Laboratory examinations include bacteriological examination of the conjunctival flora. Physiological bacterial flora contains gram positive bacteria, while gram negative bacteria are an indicator for pathological conditions. Standard reference values have been worked out for 42 different bird species from 8 orders.

5. Mydriasis and air sac perfusion anesthesia (APA)

Induction of mydriasis is indispensable for the examination of the posterior eye segment (ophthalmoscopy). A major difference between the mammalian and the avian eye however is that the commonly used mydriatic of atropine and tropicamide have little effect in the avian patient due to a striated rather than smooth intraocular musculature. Therefore the iris is partly under voluntary control. It is essential to have a dilated pupil (mydriasis) to perform an ophthalmoscopy, i. e. examination of the posterior eye segment including the vitreous, the fundus and the pecten oculi. Therefore neuromuscular blocking agents such as d-Tubocurarine (3%; 0,01-0,03 ml) may be used. As the drug penetrates the cornea insufficiently (19) it has to be administered directly into the anterior chamber by paracentesis using a 27-30 Ga needle. This technique includes substantial risk for injuries of intraocular structures causing i. a. hyphaema, increasing intraocular pressure (IOP), transmission of conjunctival flora with consecutive uveitis and systemic side effects if larger doses than recommended are used. Therefore it is recommended to use this technique just for therapeutic reasons (prevention of posterior of anterior synechia resulting from uveitis and consecutive miosis).

An alternative for routine induction of a mydriasis as well as for intraocular surgery and surgery in the head area is the air sac perfusion anesthesia. In principle APA consists of a retrograde perfusion of the lung-air sac-system through a perfusion catheter via the left caudal thoracic air sac. As a carrier gas 0,3 l/min/kg BW of O₂ and N₂O (1 : 1, min. 33 % O₂) is used. Effect of nitrous oxide application are a low potentiation of isoflurane of approx. 11 % (23) and thus improvement of the circulatory situation and release of the surgeon from isoflurane waste gases (21, 23). Higher perfusion rates than recommended result in respiratory alkalosis due to a CO₂-wash-out-effect causing severe cardiac arrhythmias. Isoflurane maintenance concentrations vary - dependent of different bird species - between 1,0 Vol. % to 2,4 Vol. % (Columba livia Gmel., 1789). Pulsoximetry is indispensable as APA causes a reversible apnea due to reduced CO₂ partial pressure causing a missing stimulation of the respiratory centre.

Advantages of APA, a long period anesthesia, which is used for routine ophthalmoscopy, electroretinography and head surgery in birds, are free surgical access to the head for intraocular surgery, stable or decreasing intraocular pressure and reversible apnea with an absolute immobilization of the patient. Achievement of mydriasis for ophthalmoscopy may be optimized by systemic administration of 0,2 mg/kg BW of the muscle relaxant Vecuronium which allows a complete mydriasis and areflexia with a lag period of approx. 26 sec. and a duration of 25 6 min. in pigeons (Columba livia Gmel., 1789) and a reduction of isoflurane consumption of approx. 25 % at the same time. This technique allows examination even of the very lens periphery with the annular pad and the fundus periphery.

6. Ophthalmoscopy

Ophthalmoscopy, a technique to examine the fundus oculi (a clinical term, describing ocular structures, which are situated behind the lens) using a focused light beam reflected from the fundus, can be carried out by both monocular and binocular and direct or indirect ophthalmoscopy in combination with double aspherical ophthalmoscopic lenses (at 30, 40, 60, 78 and 90 diopters (D, Volk Bio II) refractive power. In all cases indirect binocular ophthalmoscopy using a head ophthalmoscope is advisable. A 30 D lens is used in birds with larger pupil diameters (raptors), ophthalmoscopy of pigeons and larger psittacines requires an 78 D lens, those in small birds (canaries, budgerigars) the use of a 90 D lens. Alternatively, monocular indirect ophthalmoscopy (Ophthalmoscope 305, Leitz/Reichert) may easily performed in all birds, especially in smaller species. Up to 35 % of all traumatized birds show intravitreal hemorrhages, ophthalmoscopy therefore is obligatory in traumatized birds.

Figure 1.

Optical principles of the (monocular direct) ophthalmoscopic examination of avian eyes. Per definition "ophthalmoscopy" is the examination of ocular structures situated behind the lens, using a focused light beam directed through the pupil and performing the examination using light, reflected from the fundus oculi. For the use in birds (mainly raptors) a Finoff transilluminator serves best for this purpose. (from: Korbel R. In: König H. E., Liebich H.-G. (eds): Anatomie und Propädeutik des Geflügels. Stuttgart-New York: Schattauer Verlag 2000: 195-288.

Figure 2.

Topographical landmarks within the avian fundus with the pecten oculi and the central and temporal fovea. Accessible viewing field (bright area) using monocular direct ophthalmoscopy (taken from: (taken from: Korbel R. In: König H. E., Liebich H.-G. (eds): Anatomie und Propädeutik des Geflügels. Stuttgart-New York: Schattauer Verlag 2000: 195-288 and

Figure 3. Etiology of ocular disorders in birds-a review.

Click on image above to view a larger image.

7. Eye disorders in birds

Ocular disorders may have numerous etiologies, frequently representing ocular manifestations of systemic disorders. A review on the etiology of ocular disorders in birds is given in chart 1.

References

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2.  Korbel R, Stütz S. Fundamentals of electroretinography in the common buzzard (Buteo buteo L., 1758). Proc 2nd Sci Meet Europ College Avian Med Surg (ECAMS). London 1997:211-9.

3.  Korbel R. Diseases of the posterior eye segment. In: Lumeij JT, Redig PT, Remple JD, Lierz M, Cooper JE, (eds). Raptor Biomedicine III. Lake Worth, Florida, USA: Zool Educ Network 2000: 179-94.

4.  Korbel R. In: König H. E., Liebich H.-G. (eds): Anatomie und Propädeutik des Geflügels. Stuttgart-New York: Schattauer Verlag 2000: 195-288.

5.  Murphy CJ. Raptor ophthalmology. Compend Cont Educ Pract Vet 1987;9:241-260.

6.  Mikaelian I, Paillet I, Williams D. Comparative use of various mydriatic drugs in the kestrel (Falco tinnunculus). Am J Vet Res 1994;55:270-272.

7.  Stadtbäumer K, Korbel RT, van Wettere A, Nell B. Funktionelle Überprüfung der Tränendrüsenfunktion bei verschiedenen Vogelspezies mittels Phenolrot-Faden-Test (Zone Quick, Menicon). Proceed 13. DVG-Tagung Vogelkrht, München 2002.