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What Is Your Diagnosis?

History

A 3-month-old, captive-bred gyrfalcon (Falco rusticolus) of unknown sex was presented for acute respiratory distress and voice change of < 12-hour duration. Before presentation, the owner reported raspy vocalization after feeding. The bird had been acquired from a private breeder within weeks of hatching and was kept in a customized raptor enclosure with perches and synthetic turf in an airconditioned barn that housed a second juvenile gyrfalcon in a separate enclosure. The bird spent 2 hours daily in an outdoor flight cage covered by mosquito netting. The diet consisted of freshly killed and frozen-thawed quail (Coturnix jciponica) offered several times daily. The gyrfalcon had not yet fledged. The owner reported administering unknown dosages of mefloquine and itraconazole prophylactically as per the recommendation of a consulting veterinarian. On the day of presentation, the falcon had been administered approximately 15 mg/kg PO voriconazole as advised by the veterinarian.

On presentation, the gyrfalcon was dyspneic on inspiration and expiration. Increased respiratory effort was characterized by a tail bob, open-mouth breathing, and an orthopneic position with head and wings extended. Respiratory rate was greater than 120 breaths per minute. The bird was in thin body condition (weight = 0.83 kg) characterized by reduced pectoral musculature and a prominent keel. The rest of the physical examination was unremarkable. Evaluation of a complete blood cell count revealed a leukocytosis (white blood cell count [WBC] 65.0 X [10.sup.3] cells/[micro]L; reference interval, 2.95-9.05 X [10.sup.3] cells/[micro]L) characterized by heterophilia (49.4 X [10.sup.3] cells/[micro]L; reference interval, 1.68-6.99 X [10.sup.3] cells/[micro]L) and lymphocytosis (13.0 x 103 cells/[micro]L; reference interval, 0.64-2.35 X [10.sup.3] cells/[micro]L). (1) Results of a plasma biochemical profile revealed no significant abnormalities when compared with published reference intervals for gyrfalcons. (2,3) The gyrfalcon was kept in an oxygen chamber for 2 hours; during which time, it remained tachypneic (100 breaths per minute) until radiography could be performed with the bird under general anesthesia.

The bird was sedated with midazolam (0.25 mg/ kg IM), and anesthesia was induced with 4% isoflurane in 0.5 L/min oxygen delivered by facemask. The bird was intubated with a 4.5-mm, noncuffed endotracheal tube, and anesthesia was maintained with 2.5%--5% isoflurane in 0.5-1 L/ min oxygen with intermittent positive-pressure ventilation to maintain respiratory rate at approximately 60 breaths per minute. During anesthesia, discolored fluid and mucus occluded the endotracheal tube because of a severe productive tracheitis, requiring the tube to be removed, cleaned, and replaced several times. A swab of the mucous on the endotracheal tube was obtained for fungal culture after extubation. Right lateral and ventrodorsal radiographs were taken (Figs 1 and 2).

This case was submitted by Sarah Gronsky, BA, Peter M. DiGeronimo, VMD, MSc, and La'Toya V. Latney, DVM, Dipl ECZM (Zoo Health Management), Dipl ABVP (Reptile & Amphibian), from the Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA.

Diagnosis

Radiographs revealed a 5-cm, linear mineral opacity with soft tissue swelling to the right of the proximal trachea (Fig 1). Interclavicular, caudal thoracic, and abdominal air sacs had thickened margins, and patchy soft-tissue opacities were observed in right and left caudal thoracic and left abdominal air sacs (Fig 2)

Based on physical examination, hematologic findings, and radiographic results, the gyrfalcon was diagnosed with severe tracheitis, airsacculitis, and pneumonia, presumptively due to aspergillosis. Initial treatment included voriconazole (15 mg/ kg PO ql2h), marbofloxacin (15 mg/kg PO q24h), and meloxicam (1 mg/kg PO q24h). The falcon was kept in an oxygen cage for the next 2 days and was offered ground whole quail up to 4 times daily.

Dyspnea progressively improved over the next 3 days, but the gyrfalcon developed melena 24 hours into treatment, likely because of the stress of hospitalization. Gastroprotectants (famotidine, 0.5 mg/kg IM q24h; and sucralfate, 30 mL/kg PO) immediately before feeding, were added to the treatment plan. On day 3 after presentation, evaluation of repeat WBC revealed marked improvement of the leukocytosis (WBC, 10.6 x [10.sup.3] cells/[micro]L) with a relative heterophilia (7.31 x [10.sup.3] cells/[micro]L). The next day, results of repeat radiographs (Fig 3a) and computed tomography scan (Fig 3b) were performed with an anesthetic protocol similar to that previously described. Results showed that the linear mineral opacity lateral to the trachea remained unchanged in size, location, and position. Persistent airsacculitis characterized by mottled air sacs was also noted.

Results of computed tomography revealed round, soft tissue-attenuating nodules, 2.5-5-mm in diameter, throughout the pulmonary parenchyma and in the caudal thoracic air sacs adjacent to the margins of the parabronchi. All air sacs had thickened margins. The right epibranchial bone of the hyoid apparatus was luxated and caudoventrally displaced (Fig 4a and b).

The gyrfalcon's clinical signs resolved 4 days after presentation. The bird was eupneic with a respiratory rate of 30 breaths per minute at rest and was eating normally. No clinical signs from the luxated epibranchial bone were observed. Therefore, no treatment was pursued. The bird was discharged with oral voriconazole (15 mg/kg PO q24h) and marbofloxacin (15 mg/kg PO q24h for an additional 4 days), with instructions for cage rest for the next 4-6 weeks. After 1 week, the bird re-presented to the clinic, exhibiting dyspnea after attempted flight training. Oral examination of the gyrfalcon was unremarkable, and at no point during the course of treatment did the bird exhibit signs of dysphagia. Therefore, no further investigation of the luxated epibranchial bone was pursued. Voriconazole dosing was increased to q12h for an additional 5 weeks and doxycycline (20 mg/kg PO ql2h) prescribed for an additional 3 weeks. Several weeks into treatment, Aspergillus fumigatus infection was confirmed by fungal culture of the tracheal swab. Three months after treatment, the owner reported successful fledging, and no recurrence of clinical signs. The gyrfalcon was subsequently lost to follow up.

Discussion

Aspergillus fumigatus is a ubiquitous fungal organism, and raptors, especially gyrfalcons, are considered particularly susceptible to Aspergillus infection. (4) Clinical infection may develop secondary to several factors, including the potentially naive immune system of a juvenile patient, heavy environmental spore burden from a poorly ventilated enclosure, and long-term exposure of an arctic species to a warm and humid climate. (5) Antifungal therapy was initiated empirically before the diagnosis of aspergillosis and may have aided in this patient's ultimate recovery. (6) At presentation, the bird's clinical signs were consistent with an acute onset of severe lower respiratory disease. The position of the luxated epibranchial bone on radiographs initially caused strong speculation that it was a foreign body perforating the esophagus. Respiratory signs could have been attributed to infection descending from the cervicocephalic air sacs or to aspiration pneumonia secondary to dysphagia. Further diagnostic tests, in this case, repeated radiographs and computed tomography scans, were ultimately pursued to determine that the mineral opacity was a luxated bone of the hyoid apparatus and had no role in the observed respiratory infection. Although an incidental finding, accurate diagnosis of epibranchial bone luxation aided in the formulation of an appropriate treatment plan by excluding potentially confounding differential diagnoses. In this case, unilateral epibranchial luxation was not associated with clinical signs. The integrity of the hyoid apparatus should be considered when evaluating diagnostic imaging results of the head and neck of avian patients.

The avian hyoid skeleton functions to control and support tongue movement as well as to support the laryngeal apparatus. (7) The central axis includes the paraglossal, basihyal, and urohyal bones and articulates with the hyoid horns, comprising the ceratobranchial and epibranchial bones (Fig 4c). (8) The hyoid horns are indirectly connected to the skull by hyoid sheaths, allowing the hyoid skeleton to move independently of the jaw. (8,9) When the muscles within the hyoid sheath relax and contract, the tongue protracts and retracts allowing birds to swallow. (7,9) All avian species have a hyoid apparatus, although it has evolved differently according to the dietary and vocal needs of each species. (7,9,10) Few studies detail the function of the hyoid apparatus of raptors, but it has been suggested that falconids have a more-primitive, weaker hyoid apparatus and associated musculature compared with other species, such as hummingbirds (Trochilidae species), woodpeckers (Picidae species), and egrets (Ardeidae species). (7,11) Despite a unilaterally luxated epibranchial bone, this gyrfalcon showed no signs of anorexia, oral or cervical pain (including head tilt, depression, or paresis), or dysphagia (including dropping food or regurgitation) before presentation or throughout hospitalization. (12) This suggests the hyoid horns of gyrfalcons, and perhaps other falconids, are not essential for prehension and deglutition of food.

Because the animal's respiratory signs resolved with antifungal therapy, it is likely the luxated epibranchial bone was an incidental finding and did not contribute to the patient's clinical signs, and no treatment of the luxation specifically was pursued.

Similar injuries have been reported in a red-crowned crane (Grus japonensis) and a black African goose (Anser anser domesticus). (13,14) These birds also did not exhibit any clinical signs associated with the injured hyoid apparatus and were allowed to heal by benign neglect. In these cases, both the crane and the goose exhibited normal eating behaviors for >6 months after diagnosis, suggesting benign neglect may be the treatment of choice for birds with hyoid injury that lack clinical signs. Extraoral surgical reduction and bandaging was used to successfully treat a Chinese goose (Anser cygnoides) with a luxated hyoid apparatus. (15) In that case, surgical treatment was pursued because the luxation prevented the animal from prehending and swallowing food and water. Although surgical reduction and therapeutic bandaging were considered for the treatment of the gyrfalcon in this case, neither was pursued because of the lack of clinical signs associated with the luxation.

Given the dietary history, the luxated epibranchial bone seen by radiography was mistaken for a potential quail bone perforating the esophagus into the surrounding soft tissues. Subsequent to computed tomography and upon further questioning, the owner disclosed that the bird would frequently wedge his head through the steel bars of his enclosure and could have sustained the luxation when trying to pull his head back through the bars. The luxation was difficult to diagnose because of a general lack of familiarity of the avian skull and pharyngeal anatomy. (16,17) The raptor skull is small and triangular shaped with many small bones that often superimpose on each other during imaging, making it difficult to evaluate by radiography alone. (18) This is unlike psittacine birds, whose large, rounded skulls and voluminous beaks make it easier to identify small, delicate bone structures, such as the hyoid apparatus. (18,19) Lateral projections are recommended to evaluate the psittacine hyoid apparatus, and an oblique view of the skull can be used to successfully diagnose a fractured hyoid bone in psittacine birds. (18,19) This is more difficult in raptors because of the superimposition of these structures because of the small, pointed skull. (15) In this case, the right lateral projection allowed for radiographic evaluation of the luxated epibranchial bone, but superimposition of the endotracheal tube, mandible, and central axis of the hyoid apparatus obscured identification of the point at which the bone was luxated. Ultimately, computed tomography provided a definitive diagnosis for the radiographically observed mineral opacity by reconstructing a three-dimensional image that removed artifacts that precluded a diagnosis because of the superimposition.

References

(1.) Padrtova R, Lloyd CG. Hematologic values in healthy gyr x peregrine falcons (Falco rusticolus x Falco peregrinus). J Avian Med Surg. 2009;23(2): 108-113.

(2.) Lierz M. Plasma chemistry reference values for gyrfalcons (Falco rusticolus). Vet Rec. 2003:153(6): 182-183.

(3.) Wernick MB, Martin-Jurado O, Beaufrere H, Samour J. Plasma chemistry reference values in the gyr falcon (Falco rusticolus). Comp Clin Pathol. 2014;23(5): 1381-1386.

(4.) Joseph V. Aspergillosis in raptors. Semin Avian Exot Pet Med. 2000;9(2):66-74.

(5.) Beernaert LA. Pasmans F, Van Waeyenberghe L, et al. Aspergillus infections in birds: a review. Avian Pathol. 2010;39(5):325-331.

(6.) Di Somma A, Bailey T. Silvanose C, GarciaMartinez C. The use of voriconazole for the treatment of aspergillosis in falcons (Falco species). J Avian Med Swrg. 2007;21(4);307-316.

(7.) Johnston NE. The Avian Tongue. San Francisco, CA: Golden Gate Audubon Society; 2014.

(8.) Homberger DG. The avian tongue and larynx: multiple functions in nutrition and vocalisation. Proc Int Ornithol Congress. 1999;22:94-113.

(9.) Maina JN. The Biology of the Avian Respiratory System: Evolution, Development, Structure and Function. Cham, Switzerland: Springer International Publishing AG; 2017.

(10.) Newell SM, Roberts GD, Bennett RA. Imaging techniques for avian lower respiratory diseases. Semin Avian Exot Pet Med. 1997;6(4): 180-186.

(11.) Ladygin AV. Morpho-functional peculiarities of the hyoid apparatus in falconiformes. Zool Zhurnal. 1993;72(8):97-110.

(12.) Joseph V. Emergency care of raptors. Vet Clin North Am Exot Anim Pract. 1998; 1 (1):77 98.

(13.) Lothamer C, Snyder CJ, Mans C, et al. Treatment and stabilization of beak symphyseal separation using interfragmentary wiring and provisional bisacryl composite. J Vet Dent. 2014;31(4):255-262.

(14.) Kasaback CM. Holland M. What is your diagnosis. J Am Vet Med Assoc. 1998;213(l):27-28.

(15.) Grosset C, Sanchez-Migallon Guzman D, Waymire A, et al. Extraoral surgical correction of lingual entrapment in a Chinese goose (Anser cygnoides). J Avian Med Surg. 2013;27(4):301-308.

(16.) Smith SA, Smith BJ. Normal xeroradiographic and radiographic anatomy of the red-tailed hawk (Buteo jamaicencis) with reference to other diurnal raptors. Vet Radiol. 1990;31(6):301-312.

(17.) Wheler CL. Orthopedic conditions of the avian head. Vet Clin North Am Exot Anim Pract. 2002; 5(1):83-95.

(18.) Krautwald-Junghanns ME, Kostka VM, Dorsch B. Comparative studies on the diagnostic value of conventional radiography and computed tomography in evaluating the heads of psittacine and raptorial birds. J Avian Med Surg. 1998; 12(3): 149-157.

(19.) Paul-Murphy J, Koblik P, Stein G, Penninck D. Psittacine skull radiography. Vet Radiol. 1990:31(4): 125-131.

Please evaluate the case history, physical examination findings, and Figures 1 and 2. Based on your case assessment, formulate a differential diagnosis list, suggest any additional diagnostic tests, and develop an initial treatment plan.

Caption: Figure 1. (a) Ventrodorsal and (b) right lateral skull radiographs of a juvenile gyrfalcon that presented for acute respiratory distress and voice change.

Caption: Figure 2. (a) Ventrodorsal and (b) right lateral coelomic radiographs of the juvenile gyrfalcon described in Figure 1.

Caption: Figure 3. (a) Oblique right lateral radiograph of the skull and neck of the juvenile gyrfalcon described in Figure 1. The luxated epibranchial bone (arrow) appears as a linear, mineral opacity ventrolateral to the endotracheal tube. The other bones of the hyoid apparatus are difficult to discern because of superimposition. (b) Computed tomography, 3dimensional reconstruction of the skull and neck of the juvenile gyrfalcon. The right epibranchial hyoid bone (arrow) is luxated and displaced caudoventrally, protruding into the superficial tissues associated with the caudal aspect of the head and associated with soft tissue opacity in this area.

Caption: Figure 4. (a) Computed tomography, 3-dimensional reconstruction of the hyoid apparatus of the juvenile gyrfalcon described in Figure 1 showing luxation of the right epibranchial bone, (b) Illustration of the hyoid apparatus and luxated right epibranchial bone (Courtesy Dr L. Latney). (c) Illustration of the normal anatomy of the avian hyoid apparatus (Courtesy Dr L. Latney).
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Publication:Journal of Avian Medicine and Surgery
Date:Jun 1, 2019
Words:2599
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