Nasal adenocarcinoma and secondary chronic sinusitis in a hyacinth macaw (Anodorhynchus hyacinthinus).
Key words: adenocarcinoma, sinusitis, neoplasia, psittacine, avian, hyacinth macaw, Anodorhynchus hyacinthinus
A 20-year-old male hyacinth macaw (Anodorhynchus hyacinthinus) was presented to the Cornell University Hospital for Animals for evaluation of lethargy, nasal discharge, and dyspnea of 24 hours duration. The bird had been housed with another hyacinth macaw in a large indoor aviary for the previous 13 years. It was fed an appropriate diet (pellets and a variety of nuts, fruits, and vegetables) and received proper husbandry.
On presentation the bird was dull, moderately dehydrated (approximately 7%), and piloerect, and was open-beak breathing. A purulent, yellow discharge was present in the right naris and a serosanguineous discharge was present in the left naris. Cardiothoracic auscultation was unremarkable. The bird's body condition score was 3/5 at a weight of 1.52 kg (reference range, 1.21-1.54 kg). (1) No other abnormalities were detected on physical examination.
The bird was hospitalized for supportive care and diagnostic procedures. Results of a complete blood count (CBC) revealed severe leukocytosis (96 100 cells/[micro]L; reference mean [+ or -] SD, 7010 [+ or -] 4560 cells/[micro]L) with a severe mature heterophilia (87 500 cells/[micro]L; reference mean [+ or -] SD, 5380 [+ or -] 4270 cells/[micro]L), and a moderate anemia (36%; reference mean [+ or -] SD. 48% [+ or -] 4%). (2) Results of a plasma biochemical panel revealed a high concentration of creatine kinase (4081 U/L; reference mean [+ or -] SD, 168 [+ or -] 72 U/L) and mildly increased concentrations of aspartate aminotransferase (211 U/L; reference mean [+ or -] SD, 65 [+ or -] 13 U/L) and uric acid (9.8 mg/dL; reference mean [+ or -] SD, 4.4 [+ or -] 1.9 mg/dL). (2) A sample of the purulent nasal discharge collected directly from the left nasal cavity was submitted for aerobic bacterial culture. Treatment consisted of balanced isotonic crystalloid fluids (50 mL/kg SC q12h), enrofloxacin (15 mg/kg SC q24h; Baytril, Bayer, Shawnee Mission, KS, USA), meloxicam (0.5 mg/kg SC q24h; Metacam, Boehringer Ingelheim Vetmedica Inc, St Joseph, MO, USA), doxycycline (25 mg/kg PO q12h), and 0.9% saline nasal flushes twice daily. The next day the macaw was anesthetized for full-body orthogonal radiographs, results of which were unremarkable. A combined choanal and cloacal swab sample was submitted for polymerase chain reaction (PCR) testing for Chlamydophila psittaci.
The bird's attitude and appetite improved during the first week of hospitalization. The amount of mucous discharge and frequency of upper respiratory wheezing decreased. Despite the improvements, a bloody nasal discharge was consistently observed bilaterally (right greater than left) a few hours after sinus flushes.
Nebulization therapy with enrofloxacin (diluted to 2.25 mg/mL) and acetylcysteine (diluted to 0.1 mg/mL) was started on the fourth day of hospitalization. Additionally, acetylcysteine (diluted to 0.1 mg/mL) was added to the sinus flushes for 5 days starting on the fourth day of treatment. Treatment with an expectorant (guaifenesin, 0.8 mg/kg PO q12h) and an antihistamine (hydroxyzine, 2 mg/kg PO q12h) was also initiated.
Seven days after initial presentation, computed tomography (CT) (Toshiba Aquilion LB CT, Toshiba America Inc, New York, NY, USA) of the head was performed under general anesthesia. Before intubation, a tracheal endoscopy was performed with a 2.7-mm rigid 30-degree endoscope unit (Karl Storz Inc, El Segundo, CA, USA); no abnormalities in the tracheal mucosa or lumen were detected. Results of CT showed a large volume of soft-tissue attenuating material within the infraorbital sinus, and the preorbital diverticula were expanded bilaterally. The caudal sinuses and associated pneumatic bones appeared normal. The margin of bone where the preorbital diverticulum and calvarium met was mildly irregular and evidence of bony lysis was visible. Results of a follow-up CBC revealed severe leukocytosis with a left shift characterized by heterophilia. The packed cell volume (PCV) had decreased slightly and there was a mild polychromasia (Table 1).
The macaw continued to improve clinically and was bright and alert with an excellent appetite after 10 days of hospitalization. The mucoid nasal discharge stopped improving after the first week of treatment. Results of aerobic nasal culture revealed a mixed population of Staphylococcus intermedins and Pasteurella species, including Pasteurella pneumotropica; all isolated bacteria were susceptible to enrofloxacin. The result of Chlamydophila PCR testing was negative, and doxycycline treatment was discontinued. Gentamicin ophthalmic drops (instilled in each nostril q12h) were added to the treatment plan.
Fourteen days after presentation the macaw was anesthetized for trephination of the infraorbital sinuses. Two equidistant 5-mm holes were created between the medial canthus of each eye and the corresponding naris with a 16-gauge needle; 60 mL of sterile saline was then flushed from one trephination site to the other. The resulting serosanguineous and mucoid fluid was submitted for aerobic culture along with a piece of the frontal bone. A sterile 5-Fr red rubber catheter was cut into 2.5-cm sections, which were inserted as stents at the trephination sites and secured using 4-0 nylon suture (Ethicon Inc, Johnson & Johnson Co, Somerville, NJ, USA) in a modified finger-trap suture technique. The stents allowed for continuous drainage directly from the surgery site and provided a route to instill medication. The macaw was given butorphanol (1 mg/kg IM) for postoperative analgesia and recovered from anesthesia without complication. The stents did not seem to cause discomfort.
A CBC was repeated 17 days after presentation, and results showed no significant changes (Table 1). Cytologic examination of a nasal swab and nasal flush fluid by direct examination and cytospin showed moderate cellularity consisting of heterophils, red blood cells, and keratinized squamous epithelial cells. Chains of cocci and a single heterophil containing a phagocytized rod-shaped bacterium were also observed.
However, results of aerobic culture of a sample collected during the trephination procedure was negative for bacterial growth. After 21 days of treatment without resolution of the clinical signs, a fungal sinusitis was considered as the primary or secondary etiology. Samples of the nasal discharge were submitted for fungal culture. A blood sample was submitted for Cryptococcus fungal antigen serologic testing and an Aspergillus panel (antibody titer, serum galactomannan level, and plasma protein electrophoresis). The macaw was started on itraconazole (10 mg/kg PO q24h) and clotrimazole (1%) solution drops were instilled into both the nares and sinus stents twice daily while results were pending.
The macaw was discharged after 24 days of hospitalization. At that time, the amount of nasal discharge had decreased slightly. The sinus stents remained patent and continued to provide a route for administered medication. Treatment was continued at home and included oral enrofloxacin, itraconazole, and meloxicam. Gentamicin (0.3%) and clotrimazole (1%) drops were both administered intranasally and via the stents twice daily. At a recheck appointment 2 weeks after discharge (35 days after initial presentation), the owner reported a decreased volume of nasal discharge. Proliferation of the soft tissues around the base of the right nasal stent was noted and presumed to be a granuloma. For this reason the stents were removed. Results of the fungal culture, Cryptococcus antigen serologic testing, and Aspergillus panel were negative. Oral itraconazole and topical clotrimazole were discontinued at that time. On a recheck CBC, the PCV value had improved but the leukocytosis was more severe despite improvement in the left shift (Table 1).
The macaw was reexamined 4 weeks after discharge (50 days after the initial presentation). The bird continued to receive oral enrofloxacin, oral meloxicam, and intranasal gentamicin ophthalmic drops. The owner reported that the bird was bright, alert, and interactive but noted increased bloody discharge from both nares (right worse than left). The owner also described 2 episodes of mild, acute epistaxis. The macaw's weight continued to decrease despite a good appetite (1.33 kg, down from 1.4 kg 2 weeks previously) and it was observed to breathe solely through the oral cavity with the beak held open. A 3 x 4-mm superficial corneal ulcer was visible on the left eye and confirmed with fluorescein stain uptake. The bird was admitted to the hospital for repeat CT of the head, a CBC, and protein electrophoresis. The CT revealed the continued presence of soft-tissue attenuating material in the infraorbital sinus and associated diverticula. A circular-shaped mineral opacity was noted within the left preorbital diverticula of the infraorbital sinus (Fig 1). The chronic sinorhinopathy had also progressed to infiltrate the pneumatic portion of the caudal skull. Results of the CBC showed a worsening anemia, an improving leukocytosis, and a mild left shift (Table 1). The protein electrophoresis results revealed hypoalbuminemia (0.62 g/dL; reference mean [+ or -] SD, 2.165 [+ or -] 0.915 g/dL) and high concentrations of alpha-2 globulins (0.4 g/dL; reference mean [+ or -] SD, 0.175 [+ or -] 0.135 g/dL) and beta globulins (1.08 g/dL; reference mean [+ or -] SD, 0.46 [+ or -] 0.08 g/dL) based on normal reference intervals for macaws (Ara species). (3) Amoxicillin with clavulanate acid (125 mg/kg PO q12h) was added to the treatment protocol. Neomycin polymyxin bacitracin ophthalmic ointment (OS q8h for 7 days) was prescribed for the corneal ulcer.
Ten days after the second discharge and 60 days after the initial presentation, the bird returned for evaluation of lethargy and a change in head carriage during respiration. The owner reported that the macaw was frequently extending its neck and opening the beak during inspiration. The owner also reported frequent coughing episodes, presumed to be secondary to increased discharge from the choana into the oral cavity. Viscous discharge was observed within the beak and the volume of tan, purulent discharge from the nares had progressed in severity beyond what had been seen on previous visits. On physical examination, the macaw appeared quiet and alert. Discharge was also noted within the choana and on the caudal aspect of the tongue, just cranial to the glottis. The corneal ulcer in the left eye remained centrally located and was approximately the same size as it was on the previous visit. A decreased palpebral reflex was appreciated in the left eye. No changes to the palpebral reflex were observed in the right eye. The macaw was admitted to the hospital for supportive care and diagnostic tests. Results of a CBC showed a persistent anemia and a significantly improved leukocytosis without a left shift (Table 1). Results of the biochemical panel were within normal limits. After routine restraint for treatments on the second day of hospitalization, the macaw collapsed when placed back in the cage and went into cardiopulmonary arrest. Cardiopulmonary resuscitation was unsuccessful.
At necropsy, a poorly demarcated, 2 x 2 x 3-cm, firm, tan, friable, infiltrative mass was present in the preorbital diverticulum of the infraorbital sinus just left of midline, surrounded by a thick, yellow material (Fig 2). A thick, viscous, mucinous, white material was present at the opening of the choana, partially obstructing the airway. A similar 5X4-mm gelatinous, white, mucopurulent plug was found at the level of the syrinx, occluding both primary bronchi. Along the ventral aspect of the cranial one-third of the tracheal mucosa was a well demarcated, 4 x 0.5-cm ulcerated area covered by a slightly raised yellow plaque. The cranial lung parenchyma was diffusely firm with a rubbery consistency and mottled pink to red.
Histopathologic examination of the tracheal plaque showed severe ulceration and infiltration by macrophages and degenerate heterophils, admixed with large numbers of fungal hyphae and necrotic debris. Fungal hyphae were morphologically consistent with Aspergillus species. Examination of the cranial lung parenchyma revealed heterophilic bronchopneumonia with plant material and eosinophilic amorphous material within the airways, suggesting aspiration.
Histopathologic examination of the infraorbital sinus (Fig 3) revealed a mass composed of polygonal cells with frequent arrangement into tubular and acinar cells, structures indicative of glandular differentiation. These cells had criteria of malignancy, including marked pleomorphism with frequent large karyomegalic cells. The mitotic rate was high, with 24 mitotic figures per 10 high-power fields. The neoplasm invaded the bony turbinates of the nasal cavity, with frequent evidence of osteolysis. A few blood vessels contained clusters of neoplastic polygonal cells, consistent with vascular invasion.
Sections of processed tissues were used to detect cytokeratin within the neoplastic cells. Tissue sections cut to 5 [micro]n were mounted onto slides. The Leica Bond Polymer Refine Red Detection System (Leica Microsystems, Wetzlar, Germany) was used at manufacturer's specifications, including deparaffinization, enzyme retrieval, primary antibody incubation (DAKO CK AE1/3, 1:200 for 15 minutes), Polymer Red detection, and hematoxylin counterstain. Two trained veterinary pathologists (B.P.B. and T.S.) evaluated immunoreactivity. Immunohistochemical staining for cytokeratin (CK AE1/3) was utilized to demonstrate cellular intermediate filaments that are characteristic of cells of epithelial origin. Immunoreactivity was variable throughout the mass with 25%-50% positive cytoplasmic reactivity. Gomori-methenamine silver stain was applied to sections of the mass in an attempt to identify fungal organisms, but none were detected. Findings were interpreted as malignant adenocarcinoma with osteolysis and angioinvasion.
Neoplasia in avian species is increasingly recognized, diagnosed, and treated. In one comprehensive study, the prevalence of neoplasia in psittacine birds was 6.2%. (4) Primary respiratory neoplasia represented 9% of the cases, all of which were found to be malignant. (4) Nasal adenocarcinoma has been described previously in a conure, (5) but, to the our knowledge, this is the first report of nasal adenocarcinoma in a macaw. Neoplasms that have been reported in hyacinth macaws are bronchogenic adenocarcinoma with spinal invasion, (6) hepatic adenocarcinoma, (7) erythroblastosis of the spleen, (7) subcutaneous myelolipoma, (8) and cloacal papilloma. (9)
Sinusitis is one of the most commonly diagnosed respiratory conditions in avian patients. (10) The most common infectious causes of sinusitis are gram-negative bacteria, in particular Chlamydophila psittaci, and fungal organisms, most notably Aspergillus species. (10,11) Poor nutrition, (including hypovitaminosis A) and low humidity can predispose birds to developing sinusitis. (10) Additionally, toxins, viruses, allergies, foreign bodies, and neoplasia can also cause sinusitis. (10)
Neoplasia is an uncommon cause of sinusitis, and in this case, the macaw's initial presentation and blood test, cytologic, and imaging results did not show evidence of neoplasia; moreover, the initial presentation and findings were characteristic of a bacterial sinusitis. The absence of neoplastic cells in the cytologic samples obtained by nasal swab and flushing could be related to tumor characteristics or avian anatomical features. In psittacine birds, the solution from a nasal flush enters the nares, passes through the conchae, and exits the choana. Accessibility to the infraorbital sinus, where the tumor was located in this patient, is limited to an opening of less than 1 mm in most species, via the aperture sinus infraorbitalis. (12) Successful exfoliation of the tumor during flushing would therefore be unlikely. When the trephination procedure was performed, the evacuated fluid may have been diagnostic; however, it was not submitted for cytologic examination.
Imaging did not raise the suspicion of neoplasia because a discrete mass was not identified on radiographs or CT. On the second CT, the presence of a small amount of mineralization surrounded by attenuating material consistent with the presence of fluid or soft tissue in the infraorbital sinus was observed. This finding was attributed to chronic inflammation. In retrospect, the mineralization and associated attenuating material were caused by both chronic inflammation and the tumor identified at necropsy.
The use of magnetic resonance imaging (MRI) and intravenous contrast may have aided in identifying the tumor. Intravenous contrast may have outlined the margins of the mass and led to the suspicion of neoplasia. Additionally, MRI provides better soft-tissue resolution, lesion characterization, and anatomic localization than CT. (12) In one study, discrete lesions within the infraorbital sinus could be detected by MRI in 7 out of 10 psittacine birds suffering from chronic sinusitis. (12)
The severe leukocytosis on the initial CBC in this macaw was consistent with a bacterial sinusitis. The macaw developed a left shift after starting antibiotics rather than showing improvement in the leukocytosis. The left shift resolved; however, despite prolonged and aggressive antibiotic treatment, the leukocytosis did not decrease significantly until just before death. The lack of resolution of the leukocytosis with appropriate antibiotic treatment suggested a nonbacterial cause for the sinusitis, such as fungal infection, which was only present within the trachea at necropsy. In retrospect, it seems likely that inflammation secondary to neoplasia contributed a significant component to the persistent leukocytosis.
Antemortem diagnosis of nasal adenocarcinoma would have carried a guarded to poor prognosis. Radiation therapy is the most beneficial treatment option in dogs with nasal adenocarcinoma (13); therefore surgery would likely not have been recommended. Additionally, given the extent of the disease found at necropsy, surgical debulking would have been difficult to accomplish. Early diagnosis followed by radiation therapy would have provided the best chance of increasing the survival time of this macaw. However, there are no controlled studies to support safe and efficacious avian radiation therapy protocols.
During the course of disease, the bird developed a nonhealing ulcer of the left eye, followed by lagophthalmos. Eyelid paresis due to a cranial nerve V lesion secondary to infraorbital sinusitis has been described. (14) Fungal tracheitis was also identified in this case. The use of long-term antibiotic therapy and repeated intubation as well as prolonged illness all predisposed this patient to the development of an opportunistic fungal disease. (15,16) 10 In retrospect, beginning antifungal therapy earlier in the course of treatment might have helped prevent fungal infection. However, the macaw only received antifungal therapy concurrent with 3 out of 9 weeks of antibiotic therapy.
In one case report, an eclectus parrot (Eclectus roratus) diagnosed with squamous cell carcinoma of the infraorbital sinus also presented with fungal tracheitis, presumed to be secondary to inhalation of necrotic portions of the lesion. (17) Seeding of fungus directly from the nasal tumor in this case is unlikely as no fungal organisms were identified when Gomori-methenamine silver stain was applied to sections of the mass.
Antemortem diagnosis of adenocarcinoma of the infraorbital sinus in a psittacine bird is challenging. In this case, MRI would have had an advantage over CT but would have increased the risk to the patient because it would have prolonged the time under anesthesia. The use of intravenous contrast in combination with CT may have helped make a diagnosis and would not have significantly increased the length of the procedure. Performing cytologic examination on the fluid that was evacuated during trephination would have potentially led to a diagnosis. Additionally, the persistent, severe leukocytosis in the face of antibiotic administration was suggestive of a nonbacterial cause for the sinusitis. Neoplasia should be prioritized in cases of sinusitis that do not respond to antibiotics and supportive care.
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Brendan P. Noonan, DVM, Dipl ABVP (Avian), Ricardo de Matos, LMV, Dipl ABVP (Avian), Dipl ECZM (Avian), Brian P. Butler, DVM, MPH, PhD, Theresa L. Southard, DVM, PhD, Dipl ACVP, and James K. Morrisey, DVM, Dipl ABVP (Avian)
From the Department of Clinical Sciences (Noonan, de Matos, Morrisey) and the Animal Health and Diagnostic Center (Southard), College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA; and the Pathobiology Academic Program, School of Veterinary Medicine, PO Box 7, St George's University, St George's, Grenada, West Indies (Butler). Present address (Noonan): Angell Animal Medical Center, 350 S Huntington Ave, Boston, MA 02130, USA.
Table 1. Summary of CBC results performed from an adult hyacinth macaw during the course of treatment for presumed bacterial sinusitis. Days following presentation CBC Day 1 Day 7 Day 10 Day 17 PCV (%) 36 28 30 26 WBC ([10.sup.3] cells/[micro]L) 96.1 65.7 45.8 60.6 Heterophils ([10.sup.3] cells/[micro]L) 87.5 55.8 33 44.8 Band heterophils ([10.sup.3] cells/[micro]L) 0 4.6 0 0 Lymphocytes ([10.sup.3] cells/[micro]L) 6.7 2.6 7.8 13.3 Monocytes ([10.sup.3] cells/[micro]L) 0 1.3 0.5 0.6 Eosinophils ([10.sup.3] cells/[micro]L) 1 1.3 2.3 1.2 Basophils ([10.sup.3] cells/[micro]L) 1 0 2.3 0.6 Platelets (cells/100 WBCs) Adequate Adequate Adequate Adequate Total protein (g/dL) 3.7 3.6 3.7 4.6 Days following presentation CBC Day 22 Day 35 Day 50 Day 60 PCV (%) 28 34 27 27 WBC ([10.sup.3] cells/[micro]L) 55.4 58.8 39.3 35.3 Heterophils ([10.sup.3] cells/[micro]L) 26 37.6 29.5 27.5 Band heterophils ([10.sup.3] cells/[micro]L) 23.3 18.8 4.7 0 Lymphocytes ([10.sup.3] cells/[micro]L) 5 1.2 2.4 3.9 Monocytes ([10.sup.3] cells/[micro]L) 0.6 0.6 1.6 1.8 Eosinophils ([10.sup.3] cells/[micro]L) 0.6 0.6 1.2 1.8 Basophils ([10.sup.3] cells/[micro]L) 0 0.6 0 0.4 Platelets (cells/100 WBCs) Adequate Adequate Adequate Adequate Total protein (g/dL) 5 4.3 3.8 3.5 Reference mean CBC [+ or -] [SD.sup.2] PCV (%) 48 [+ or -] 4 WBC ([10.sup.3] cells/[micro]L) 7.01 [+ or -] 4.56 Heterophils ([10.sup.3] cells/[micro]L) 5.38 [+ or -] 4.27 Band heterophils ([10.sup.3] cells/[micro]L) 0 Lymphocytes ([10.sup.3] cells/[micro]L) 1.22 [+ or -] 0.89 Monocytes ([10.sup.3] cells/[micro]L) 0.12 [+ or -] 0.15 Eosinophils ([10.sup.3] cells/[micro]L) 0.05 [+ or -] 0.07 Basophils ([10.sup.3] cells/[micro]L) ND Platelets (cells/100 WBCs) 8.8 [+ or -] 3.3 Total protein (g/dL) 3.5 [+ or -] 1.5 Abbreviations: CBC indicates complete blood count; PCV, packed cell volume; WBC, white blood cell; ND, not detectable.
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|Author:||Noonan, Brendan P.; de Matos, Ricardo; Butler, Brian P.; Southard, Theresa L.; Morrisey, James K.|
|Publication:||Journal of Avian Medicine and Surgery|
|Article Type:||Case study|
|Date:||Jun 1, 2014|
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