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Bilateral granulomatous and fibrinoheterophilic otitis interna due to Pseudomonas aeruginosa in a captive little bustard (Tetrax tetrax).

Abstract: A captive juvenile little bustard (Tetrax tetrax) was presented for acute onset of right head tilt and right circling. The bird failed to respond to supportive care and systemic antibiotic therapy. A bilateral granulomatous and fibrinoheterophilic otitis interna due to Pseudomonas aeruginosa was diagnosed postmortem by histopathologic examination and bacterial culture. In bustards, Pseudomonas species have been documented in the normal bacterial flora of the oropharynx and are frequently reported in upper respiratory tract infections. This is the first report of a peripheral vestibular syndrome due to P aeruginosa otitis interna in a bustard species. Pseudomonas aeruginosa should be included as a possible cause of otitis and peripheral vestibular syndrome in bustards.

Key words: Pseudomonas aeruginosa, otitis interna, vestibular syndrome, avian, little bustard, Tetrax tetrax.

Clinical Report

A 2-month-old male little bustard (Tetrax tetrax) was presented by animal keepers because of an acute onset of a right head tilt. The bird had been hand-fed since hatching with several other bustards as part of a reproduction program.

On initial examination (day 0), the bird was standing but unsteady on its legs with mild loss of balance, trembling, and drooped wings. The bird's head was rotated toward the right side, and circling toward the right was observed. Weight loss (370 g) was noticed compared with the weight recorded 1 week before (410 g), and body condition score was poor (2/5). External auditory meatus appeared normal on examination. No other anomalies were present on physical examination.

A blood sample was collected from the right jugular vein for hematologic analysis. Values were compared with reference intervals established for 8-12-week-old houbara bustards (Chlamydotis undulata). (1) A severe leukocytosis (35.7 x [10.sup.3] cells/[micro]L; reference interval, 8.77 [+ or -] 0.55 x [10.sup.3] cells/[micro]L) due to heterophilia (30.4 x [10.sup.3] cells/[micro]L; reference interval, 3.87 [+ or -] 0.6 x [10.sup.3] cells/[micro]L) and monocytosis (2.2 x [10.sup.3] cells/[micro]L; reference interval, 0.42 [+ or -] 0.07 x [10.sup.3] cells/[micro]L) was present. Therefore, an infectious cause was initially suspected. No other anomalies were present on blood analysis.

The initial treatment plan included providing a source of heating, force-feeding 3 times a day, and providing supplemental vitamin E (1 mg IM q24h), and 5% glucose (5 mL SC q12h). Antibiotic treatment consisted of trimethoprim sulfamethoxypyridazine (30 mg/kg IM q12h) and enrofloxacin (15 mg/kg IM q12h; Baytril 5%, Bayer Sante Animale, Puteaux, France). Butorphanol (1 mg/kg IM q12h; Torbugesic 1%, Fort Dodge Sante Animale) and meloxicam (1 mg/kg IM once then PO q12h) were also prescribed.

On day 1, neurologic signs worsened, with more severe right circling and right head tilt. Additions to the treatment plan included dexamethasone (1 mg/kg IM once), amoxicillin clavulanic acid (125 mg/kg PO q12h), and itraconazole (10 mg/kg PO q12h; Itrafungol, Janssen Sante Animale, Issy-Les-Moulineaux, France) for aspergillosis prevention or in case of a mycotic infection. Because the bustard was losing weight, force-feeding frequency was increased to q6h. On day 2, the bird was stable, with the severity of the vestibular syndrome unchanged. Treatment was continued with the addition of vincamine and papaverine chlorhydrate (0.15 mL/kg IM once; Candilat, Laboratoire TYM, Lempdes, France) for cerebral vasodilatation effects in case of vascular disease.

On day 3, the bird was found dead in the morning, and a complete necropsy was immediately performed. Macroscopically, the only anomaly observed was an asymmetry of the tympanic bullae; the left tympanic bulla appeared normal, whereas the right had an irregular surface and was larger in diameter (5 mm versus 3 mm). Tissue samples were fixed in 10% phosphate-buffered neutral formalin, routinely processed, and stained with hematoxylin and eosin for histopathologic examination. Architecture of both inner ears was obliterated by a granulomatous and fibrinoheterophilic process characterized by an accumulation of viable and degenerate heterophils, fibrin, necrotic debris, and activated macrophages (Fig 1). No pathogens were seen with hematoxylin and eosin or special stains (periodic acid-Schiff and Ziehl Neelsen), but Gram's stain results showed gram-negative coccobacilli in the center of the lesions and in the cytoplasm of macrophages and heterophils (Fig 2). The fibrinoheterophilic inflammation extended into the underlying bone, with associated severe osteoproliferative changes. No significant lesions were seen in other organs. These lesions were compatible with a severe bilateral granulomatous and fibrinoheterophilic otitis interna; a bacterial etiology was highly suspected. Culture from a sterile swab of the osseous mass of the right inner ear revealed pure growth of Pseudomonas aeruginosa.

Discussion

The little bustard belongs to the family Otididae and to the order Otidiformes. This bird is terrestrial and inhabits dry grasslands from European Mediterranean and southwest Asian countries. This species is listed as Near Threatened since 2004 by the International Union for Conservation of Nature because of rapid overall population decline, mainly because of habitat loss and degradation. (2) Bustard medicine has been intensively described elsewhere. (1,3) The most common causes of death in adult captive bustards are related to trauma and capture myopathy. In juveniles, mortalities most often result from yolk-sac infection, gram-negative bacterial septicemia, gastrointestinal tract obstruction, and nutritional bone disease. (4)

The present case is the first report of a peripheral vestibular syndrome due to P aeruginosa otitis interna in a bustard species. Several causes have been described for head tilt in birds. The origin of the lesion can be central or peripheral. Peripheral origins of vestibular syndrome such as traumatic lesions (bone fracture, or trauma to the eighth cranial nerve) or infectious diseases of the inner ear have been described. (5,6) Central origins of vestibular syndrome include neoplasia, parasites, and infectious diseases. (6,7) Paramyxovirus type 1 is the only viral etiology of encephalitis with head tilt reported in bustards. (8) Other causes of vestibular syndrome include toxicosis and nutritional disease (hypovitaminosis E). (6) Otitis (externa, media, or interna) has been rarely described in birds. (9)

Potential causes of otitis externa are infectious diseases (bacteria, viruses, fungi, and parasites), and neoplastic process (carcinoma of the glands of the external ear canal, squamous cell carcinoma). (10,11) Otitis media may be secondary to an otitis externa, a penetration of the tympanic membrane by a foreign body, an extension of nasopharyngeal infection via the pharyngotympanic tube, (10) or to an inflammation of the air spaces of the surrounding bone. Causes of otitis interna include viruses (paramyxovirus, poxvirus), (10) bacteria (Salmonella enterica subsp arizonae in turkeys, (9) Ornithobacterium rhinotracheale in partridges [Alectoris rufa]), (5) ototoxicity by some antibiotics, (10,12) and trauma. (10)

Pseudomonas aeruginosa is a motile, strictly aerobic, gram-negative, rod-shaped bacterium with a worldwide distribution. (13) This bacterium is a saprophyte in aquatic environments and moist soil. In avian species, it is considered an opportunistic pathogen. (6,11,13) Predisposing risk factors are stress, drinking water contaminated by organic matter, and concurrent infections. (1) In this bustard, no predisposing factors were identified. In birds, P aeruginosa has been isolated in cases of conjunctivitis, (14) upper respiratory tract infections in poultry, (6) corneal ulcers in cranes, (15) salt gland infection in ducks, (16) enteritis, septicemia, (6) and otitis media in African grey parrots (Psittacus erithacus). (17) In bustards, P aeruginosa has mainly been isolated in upper respiratory tract infections in adults and juveniles, causing conjunctivitis, rhinitis, sinusitis, laryngitis, and tracheitis. (1,18) Pseudomonas aeruginosa has also been described in bustards with yolk-sac infection, meningitis and septicemia, (1) and more sporadically in dermatitis, panopthalmitis, osteomyelitis, hemorrhagic diarrhea, and stomatitis. (1,18) Chicks are very susceptible to P aeruginosa infection with acute evolution and high mortality rate. (1)

Bacterial otitis interna can lead to meningitis with bacteria spreading through the vestibulocochlear nerve. (9) Occasionally, otitis media can progress to otitis interna and then to meningitis. (5) Hematogenous spread of infection to the inner ear is considered rare. (19) In this bustard, the exact origin of the inner ear infection was not determined. In absence of meningitis and pharyngitis, bacteria may have originated from the external auditory canal without otitis externa. The foraging behavior of bustards may predispose these birds to ear contamination with foreign bodies and gram-negative bacteria from the soil. (14) A second hypothesis is an ascending infection of the middle and inner ears through the auditory canals in an asymptomatic carrier, since Pseudomonas species has been described as normal bacterial flora of the oropharynx in bustards. (20) We favor this second hypothesis because of the bilateral localization of the infection. In this case, the histopathologic findings were compatible with a subacute infectious process. The vestibular syndrome appeared suddenly, but the weight loss observed over 1 week suggests dysorexia several days before the head tilt. The right head tilt can be explained by the more severe macroscopic lesion of the right inner ear compared with the left ear. The cause of death may be related to the stress of hospitalization because no signs of septicemia, encephalitis, or myocarditis were observed. Nevertheless, an intolerance to vincamine and papaverine chlorhydrate could not be excluded, as the safety of these drugs has not been studied in birds.

Treatment of P aeruginosa infection is difficult because this bacterium presents resistance to numerous antibiotics. This resistance is provided by plasmids, a nonpermeable external membrane, and production of enzymes that deteriorate [beta]-lactams and aminoglycosides. (21) In the present case, enrofloxacin, trimethoprim sulfamethoxypyridazine, and amoxicillin-clavulanic acid were used, but most P aeruginosa are considered resistant to trimethoprim-sulfonamide and amoxicillin-clavulanic acid, and also to several cephalosporins, macrolides, rifampicin, erythromycin, amphenicols, and tetracycline. (21,22) Fluoroquinolones, ceftazidime, piperacillin, neomycin, tobramycin, amikacin, and gentamicin are considered effective, (21,22) but resistance to gentamicin has sometimes been reported. (23) This bustard failed to respond to systemic enrofloxacin treatment, which can be explained by infection of tissues where antibiotic effective concentration could not be reached, (9) but resistance to enrofloxacin could not be ruled out because an antibiogram was not performed. The chronicity of the lesions may have impaired response to treatment as well.

In the present case, a bilateral bacterial otitis interna was diagnosed postmortem in a captive juvenile little bustard. The right head tilt appeared acutely despite chronic ear lesions being present. Infection caused by P aeruginosa should be included in the differential diagnosis of vestibular syndrome and as a possible cause of otitis interna in bustards.

References

(1.) Bailey TA. Diseases and Medical Management of Houbara Bustards and Other Otididae. Abu Dhabi, United Arab Emirates: National Avian Research Center; 2007.

(2.) BirdLife International. Tetrax tetrax. IUCN Red List of Threatened Species Web site. Version 2011.2. http://www.iucnredlist.org. Accessed November 2011.

(3.) Bailey TA. Veterinary care of bustards. In: Fowler ME, Miller RE, eds. Zoo and Wild Animal Medicine. Current Therapy 6. St. Louis, MO: Saunders Elsevier; 2008:170-185.

(4.) Bailey TA, Nicholls PK, Samour JH, et al. Postmortem findings in bustards in the United Arab Emirates. Avian Dis. 1996;40(2):296-305.

(5.) Moreno B, Chacon G, Villa A, et al. Nervous signs associated with otitis and cranial osteomyelitis and with Ornithobacterium rhinotracheale infection in red-legged partridges (Alectoris rufa). Avian Pathol. 2009;38(5):341-347.

(6.) Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers; 1994.

(7.) Lopez RM, Murcia DB. First description of malignant retrobulbar and intracranial teratoma in a lesser kestrel (Falco naumanni). Avian Pathol. 2008;37(4):413-414.

(8.) Bailey TA, Nicholls PK, Wernery U, et al. Avian paramyxovirus type 1 infection in houbara bustards (Chlamydotis undulata macqueenii): clinical and pathological findings. J Zoo Wildl Med. 1997;28(3):325-330.

(9.) Shivaprasad HL, Cortes P, Crespo R. Otitis interna (labyrinthitis) associated with Salmonella enterica arizonae in turkey poults. Avian Dis. 2006;50(1):135-138.

(10.) Schmidt RE, Reavill DR, Phalen DN, eds. Pathology of Pet and Aviary Birds. Ames, IA: Blackwell Publishing; 2003.

(11.) Altman RB, Clubb SL, Dorrestein GM, Quesenberry K, eds. Avian Medicine and Surgery. Philadelphia, PA: WB Saunders; 1997.

(12.) Selimoglu E. Aminoglycoside-induced ototoxicity. Curr Pharm Des. 2007; 13(1): 119-126.

(13.) Quinn PJ, Carter ME, Markey BK, et al. Clinical Veterinary Microbiology. London, United Kingdom: Mosby International; 1994.

(14.) Silvanose CD, Bailey TA, Naldo JL, Howlett JC. Bacterial flora of the conjunctiva and nasal cavity in normal and diseased captive bustards. Avian Dis. 2001;45(2):447-451.

(15.) Miller PE, Langenberg JA, Hartmann FA. The normal conjunctival aerobic bacterial flora of three species of captive cranes. J Zoo Wildl Med. 1995;26(4):545-549.

(16.) Klopfleisch R, Muller C, Polster U, et al. Granulomatous inflammation of salt glands in ducklings (Anas platyrhynchos) associated with intralesional gram-negative bacteria. Avian Pathol. 2005;34(3):233-237.

(17.) Munger LL, Pledger T. Pseudomonas infection of the middle ear. Proc Annu Conf Assoc Avian Vet. 1993:254-255.

(18.) Bailey TA, Naldo J, Samour JH, et al. Bustard pediatric diseases: a review of clinical and pathologic findings. J Avian Med Surg. 1997; 11(3): 166-174.

(19.) Kahn CM, Line S, eds. The Merck Veterinary Manual. 10th ed. Whitehouse Station, NJ: Merck Publisher; 2010.

(20.) D'Aloia MA, Bailey TA, Samour JH, et al. Bacterial flora of captive houbara (Chlamydotis undulata), kori (Ardeotis kori) and rufous-crested (Eupodotos ruficrista) bustards. Avian Pathol. 1996;25(3):456-468.

(21.) Euzeby JP. List of prokaryotic names with standing in nomenclature. List of Prokaryotic Names With Standing in Nomenclature (LPSN) Web site, http://www.bacterio.cict.fr/. Updated September 2013. Accessed November 2011.

(22.) Schildger BJ, Zschock M, Gobel T. O-serovar distribution and antibiotic sensitivity of Pseudomonas aeruginosa strains from birds and reptiles. Zentralbl Veter inarmed B. 1989;36(4):292-296.

(23.) Samour JH. Pseudomonas aeruginosa stomatitis as a sequel to trichomoniasis in captive saker falcons (Falco cherrug). J Avian Med Surg. 2000;14(2):113-117.

Christopher Scala, DVM, Isabelle Langlois, DVM, Dipl ABVP (Avian), and Karin Lemberger, DVM, Dipl ACVP

From the Reserve de la Haute-Touche, Museum National d'Histoire Naturelle, 36290 Obterre, France (Scala); Department of Clinical Sciences, Zoological Medicine Service, Faculte de medecine veterinaire, Universite de Montreal, 3200 rue Sicotte, Qc J2S 2M2 Saint-Hyacinthe, Canada (Langlois); and Vet Diagnostics, 14 avenue Rockefeller, 69008 Lyon, France (Lemberger). Present address (Scala): Department of Clinical Sciences, Zoological Medicine Service, Faculte de medecine veterinaire, Universite de Montreal, 3200 rue Sicotte, Qc J2S 2M2 Saint-Hyacinthe, Quebec, Canada.
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Title Annotation:Clinical Report
Author:Scala, Christopher; Langlois, Isabelle; Lemberger, Karin
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Jun 1, 2015
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