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Conjunctival flora in tawny owls (Strix aluco)
  1. G. O. Cousquer, BSc, BVM&S, CertZooMed, PGDOE, MSc, MRCVS1,1,
  2. J. E. Cooper, BVSc, DTVM, CBiol, FIBiol, FRCPath, DiplECVP, CertLAS, FRCVS2 and
  3. M. A. Cobb, MA, VetMB, DVC, PhD, MBA, MRCVS3
  1. 1 CertZooMed, PGDOE, MSc, MRCVS, RSPCA Wildlife Hospital, West Hatch, Taunton, Somerset TA3 5RT
  2. 2 Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES
  3. 3 School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD
  1. E-mail for correspondence: glencousquer{at}hotmail.com

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INJURIES to the anterior segment of the eyes are commonly seen in free-living tawny owls (Strix aluco) admitted to wildlife rehabilitation centres. Pathology affecting only the surface of the eye was reported in almost 25 per cent of adult free-living tawny owls that received an ophthalmological examination on admission to the RSPCA's West Hatch Wildlife Hospital in south-west England (Cousquer 2005). Of the 103 adult birds examined as part of that study, 26 had corneal lesions. However, no infectious causes of this corneal pathology were demonstrated. Four owls had fallen down a chimney and soot contamination, is likely to have caused damage to the ocular tissues of these birds. In the remaining cases, it was suggested that most of the corneal ulceration observed also arose through trauma. Mention was also made of the possible involvement of tear film break-up and exposure keratopathy in dehydrated birds, together with movement over the unprotected cornea of the third eyelid. Williams and others (2006) reported persistent corneal ulceration in 20 of 100 eyes of 12 of 50 tawny owls kept in long-term captivity in two rehabilitation centres. A further 14 eyes (seven birds) demonstrated corneal scarring with lipid keratopathy. The corneal pathology reported was attributed to trauma, and it was suggested that persistent lesions arose where trauma produced a devitalised area of anterior stroma that was not conducive to re-epithelialisation. The fact that such a high number of tawny owls were retained in captivity as a result of their corneal pathology, rather than being released back to the wild, illustrates how important the early management of such lesions is to the successful treatment and rehabilitation of casualty owls.

Corneal injuries can become secondarily infected by opportunistic bacteria. Knowledge of the conjunctival flora is likely to prove useful in directing the medical treatment of such injuries. This short communication provides information on the bacterial flora recovered from the eyes of tawny owls following conjunctival swabbing. The findings are intended to guide practitioners dealing with wild bird casualties in the selection of appropriate therapeutic agents.

A total of 39 adult tawny owls were examined as part of the study. They were all presented to the RSPCA's West Hatch Wildlife Hospital during 2001 and 2002. All adult owls admitted to the hospital during this time were, where practically possible, recruited to the study, regardless of the reason for presentation or injuries.

Each tawny owl was investigated ophthalmologically as part of its physical examination. A more extensive examination was then performed under general anaesthesia. As part of the evaluation, a fresh, saline-moistened urethral swab was inserted into the lower conjunctival fornix of each eye as described for rabbits by Cooper and others (2001). The eyelid margin and feathers were avoided. Swabs were placed in charcoal transport medium and then submitted by post to Greendale Veterinary Laboratories, Surrey, for bacterial culture and sensitivity testing.

Bacterial flora from each swab were plated on to Columbia blood agar (CM0331; Oxoid) and 5 per cent defibrinated sheep blood and MacConkey's agar without salt (CM0507; Oxoid). The plates were incubated overnight at 37°C. Any bacteria grown were identified using standard techniques (colony and microscopic morphology, Gram stain and API [bioMńrieux]) and recorded. Where no growth was obtained, the plates were reincubated for a further day. If bacterial growth was obtained, it was identified as per the techniques described above. If no growth was obtained then this was recorded. For each bacterial species or strain isolated, an antibiotic sensitivity test was carried out, by disc, on Iso-sensitest agar (CM471; Oxoid) for the following antimicrobial agents: chloramphenicol, enrofloxacin, gentamicin, neomycin, oxytetracycline, fusidic acid, trimethoprim/sulfamethoxazole, framycetin and cefalexin.

Twenty of the 39 owls were admitted following a suspected road traffic accident. Two owls had flown into a window, one had been caught on a barbed wire fence and a further five had been caught in netting. Of the remaining 11 owls, one had been found locked in a barn, three had wing injuries, three were found on the ground and four did not have a known or recorded reason for admission.

Swabs were collected from both the left and the right eye of 38 owls included in the study; one bird was excluded because only one of its eyes had been swabbed. This occurred at the start of the study when the sampling protocol had not been finalised.

Corneal pathology was seen in 25 of the 38 tawny owls (65.8 per cent). Of the 25 birds presenting with corneal pathology, nine had lesions in both eyes, five had lesions in the left eye only and 11 had lesions in the right eye only. Of the 25 birds with lesions, 18 had scratches to the cornea and the other seven had more extensive ulceration.

Two (5.3 per cent) of the 38 birds yielded no bacterial growth. A number of different organisms were cultured from the eyes of the remaining 36 birds (Table 1). Pure growths were obtained in 24 (66.7 per cent) of these 36 birds; mixed growths or growths differing between the right and left eye characterised the remaining 12 (33.3 per cent) of the birds.

Of the 24 birds yielding a pure growth from both eyes, 20 (83.3 per cent) isolates were of Staphylococcus aureus, three (12.5 per cent) were of Staphylococcus epidermidis and one (4.2 per cent) was of an Enterobacter species.

Of the 12 birds providing a mixed growth, S aureus was isolated from six birds and S epidermidis from three birds. One of these birds yielded only a light growth of S aureus from the left eye and no growth from the right. In addition, Escherichia coli was isolated from six birds, Pseudomonas aeruginosa from one bird (in conjunction with S aureus), a yeast species from one bird (in conjunction with S epidermidis), an Enterobacter and a Bacillus species from one bird (in conjunction with E coli), an Enterococcus species from two birds and a Streptococcus species from two birds. The mixed growth comprising an Enterobacter species, a Bacillus species and E coli was associated with myiasis of the eyes and periocular tissues. The association between these isolates and the presence of corneal scratches and ulceration is shown in Table 1.

Sensitivity results were obtained for 44 of the 50 isolates reported in Table 1. These sensitivity results are shown in Table 2. S aureus was most sensitive to gentamicin (100 per cent of isolates), framycetin (100 per cent of isolates) chloramphenicol (96.2 per cent of isolates), enrofloxacin (96.2 per cent of isolates), neomycin (92 per cent of isolates) and fusidic acid (87.5 per cent of isolates). Resistance was observed to fusidic acid in five isolates, although two of these were obtained from birds in which a second isolate was sensitive to fusidic acid. Resistance to oxytetracyline was observed in four of 13 (30.8 per cent) cases. The six S epidermidis samples tested for their resistance to enrofloxacin, neomycin and framycetin, and the five samples tested against fusidic acid and gentamicin, were all sensitive. Sensitivity was lower for chloramphenicol (66.7 per cent of isolates) and oxytetracycline (83.3 per cent of isolates). All six E coli isolates tested were sensitive to chloramphenicol, enrofloxacin, neomycin and framycetin, and the five isolates tested against gentamicin and oxytetracycline also demonstrated 100 per cent sensitivity. By contrast, all six also demonstrated resistance to fusidic acid.

Corneal pathology is a common finding in casualty tawny owls, and requires urgent and appropriate treatment if the corneal epithelium is to repair itself and the bird be released back to the wild.

It has been suggested that a deficiency in the tear film may predispose to the development of corneal erosions (Cousquer 2005). In birds with persistent corneal lesions, higher rather than lower modified Schirmer tear test readings were reported (Williams and others 2006). An increase in tear production may therefore occur in the presence of painful corneal ulceration, while low tear production may contribute initially to the development of the lesions.

S aureus was the most common isolate from tawny owl eyes, both those with and without corneal pathology. The origin of this organism may be the bird itself, as S aureus is commonly found as part of the resident conjunctival flora of raptors, including owls (Dupont and others 1994, Cooper 2002), bustards (Silvanose and others 2001) and various other birds (Wolf and others 1983). Dupont and others (1994) suggested that staphylococcal organisms, as part of the flora inhabiting the external surface of the cornea, protect the eye by competing for nutrients with any invading organisms and producing in some way substances with antimicrobial properties. The healthy flora can, however, become pathogenic, particularly where the immune defence mechanisms of the host are compromised.

Gram-positive organisms are usually the predominant microorganisms in healthy avian eyes, with coagulase-negative staphylococci predominating (Zenoble and others 1983, Dupont and others 1994). The findings reported in the present study are therefore consistent with previous publications.

Good sensitivity was demonstrated to most of the antibiotics tested. In practice, the need to handle and medicate owls as infrequently as possible demands that a once-daily treatment be selected. Fusidic acid (Fucithalmic; Leo Laboratories) is therefore a common first-choice antibiotic. It should be noted that almost 20 per cent of the isolates of S aureus demonstrated resistance to fusidic acid. This may not be of great concern, however, as the concentration of antibiotic in discs used to determine disc sensitivity generally equates to concentrations achieved with systemic use. The concentration of fusidic acid in the tear film following topical use will be much higher than that achieved systemically and can generally be expected to exceed the minimal inhibitory concentrations (MICs) of most Gram-positive organisms, even where they are assessed as resistant on disc sensitivity testing. McLellan and others (2002) reported concentrations of sodium fusidate in the tear fluid of clinically normal mixed-breed cats of 2.49 mg/l at two hours, 4.41 mg/l at six hours, 0.47 mg/l at 12 hours and 1.62 mg/l at 24 hours following topical application. With the exception of the 12 hours post-treatment reading, these concentrations all exceeded the MIC90 of the Staphylococcus species typically isolated from cases of feline conjunctivitis. Tissue concentrations achieved within the conjunctiva were also significant, while those achieved within corneal tissue were considerably lower. It is difficult to extrapolate from these results in cats to tawny owls. While it appears likely that high concentrations of fusidic acid may be established in the tear fluid of these birds, any tear film deficiency may have a negative bearing on the therapeutic result. In addition, the concentration achieved in corneal tissue is of interest here, as corneal ulceration, not conjunctivitis, is the primary problem requiring treatment.

There appears to be no information available on the MIC values of the staphylococcal organisms typically isolated from tawny owls. Such information would be required in order to further evaluate the efficacy of topical fusidic acid in the treatment of corneal ulceration in tawny owls. It should also be noted that these results are based on a small population of free-living birds from south-west England and may not be representative of the situation elsewhere in the UK. In view of these limitations, response to treatment should be monitored carefully. Where a treatment failure is suspected, the eye should be swabbed for culture and sensitivity testing, and treatment should be switched to an aminoglycoside such as gentamicin (Tiacil; Virbac) pending receipt of the results.

All E coli isolates identified were resistant in vitro to fusidic acid. It is likely that this organism is a contaminant that is introduced into the eye when the bird is injured and comes into contact with the ground. This is in keeping with the proposed pathogenesis of bumblefoot in birds of prey (Cooper 2002). In one case reported here, the presence of E coli was associated with fly larvae. Where such contamination is suspected, topical treatment should favour a treatment known to be effective against Gram-negative organisms.

Acknowledgements

The generous financial support of Leo Laboratories is gratefully acknowledged. The authors also thank the staff of the West Hatch Wildlife Hospital and Greendale Veterinary Laboratories.

References

Footnotes

  • Mr Cousquer's present address is Moray House School of Education, University of Edinburgh, St Leonard's Land, Holyrood Road, Edinburgh EH8 8AQ

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