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Antemortem diagnosis and successful treatment of pulmonary candidiasis in a sun conure (Aratinga solstitialis).

Abstract: An adult male sun conure (Aratinga solstitialis) was evaluated because of lethargy, ruffled feathers, and decreased appetite. Physical examination revealed hypothermia, dehydration, dyspnea, and crop distention. Results of a complete blood cell count revealed a marked inflammatory leukogram, and cytologic examination of a crop swab sample identified gram-negative bacilli and occasional yeast organisms. Radiographs demonstrated an opaque, ill-defined, soft tissue structure in the caudal coelom just cranial to the renogonadal silhouette, loss of serosal detail, and splenomegaly. Endoscopic examination revealed a pale, granuloma-like structure within the caudal aspect of the left lung, splenomegaly, and an enlarged proventriculus. Intraoperative cytologic examination of a biopsy sample of the lesion demonstrated yeast organisms, and a subsequent culture of the biopsy sample revealed Candida albicans. The bird was treated intraoperatively with intralesional amphotericin B. Postoperative treatment consisted of meloxicam, trimethoprim sulfa, amphotericin B by nebulization, and systemic itraconazole and fluconazole. The bird made a complete recovery, was discontinued from all medications, and has remained asymptomatic for 6 months. Although rare, pulmonary candidiasis should be on the list of differential diagnoses for any respiratory infection in birds. Endoscopic biopsy, cytology, and fungal culture were valuable in making the diagnosis.

Key words: pulmonary candidiasis, Candida albicans, fungal pneumonia, avian, sun conure, Aratinga solstitialis

Clinical Report

An adult male sun conure (Aratinga solstitialis) was presented for emergency care (day 1) because of acute onset of lethargy, ruffled feathers, and a 2-week history of inappetence after an abrupt dietary change. The conure had no history of contact with any other birds. Physical examination revealed a body weight of 124 g, body condition score of 2.5/ 5, hypothermia (38.8[degrees]C [101.8[degrees]F]; reference interval body temperature for birds, approximately 40[degrees]C-44[degrees]C [104[degrees]F-111.2[degrees]F]), (1) lethargy, dehydration (estimated at 7%), dyspnea, a crust over the right nostril, and a crop distended with fluid and gas. A blood sample was collected from the right jugular vein for hematologic testing and biochemical analysis before treatments. Crop lavage was performed with sterile saline, and a Gram-stain of a smear of crop contents revealed few gram-positive bacilli and few nonbudding yeast organisms (less than 5 per X100 objective field).

The bird was hospitalized in an incubator maintained at 29.4[degrees]C (85[degrees]F) and received supportive fluid therapy with lactated Ringer's solution (120 mL/kg per day SC) and gavage feeding (2.4 kcal per day, Emeraid Omnivore-Avian, Lafeber Co, Cornell, 1L, USA). Additional treatments with trimethoprim sulfa (50 mg/kg PO q12h), meloxicam (0.5 mg/kg PO q12h), and nystatin (400 000 IU/kg PO q12h) were also added. However, only mild clinical improvement was observed within the first 24 hours.

[FIGURE 1 OMITTED]

Results of hematologic testing revealed a severe leukocytosis of 60 900 cells/[micro]L (reference interval, 4000-11 000 cells/[micro]L; all reference intervals, Comparative Pathology Laboratory, University of Miami School of Medicine, Miami, FL, USA]), with a predominant heterophilia of 53 600 cells/[micro]L (reference interval, 2200-8250 cells/[micro]L), eosinophilia of 1200 cells/[micro]L (reference interval, 0-220 cells/[micro]L), and monocytosis of 2400 cells/[micro]L (reference interval, 0-220 cells/[micro]L), consistent with a marked inflammatory leukogram. Results of plasma biochemical analysis revealed high activity of aspartate aminotransferase (871 U/L; reference interval, 125-345 U/L) and high concentrations of sodium (161 mEq/L; reference interval, 134-149 mEq/L), creatine kinase (2196 U/L; reference interval, 35-355 U/L), and potassium (>8.5 mEq/L; reference interval, 3.4-5 mEq/L); however, a 24- sample hemolysis most likely caused interference with the analysis. Results of bile acids, calcium, glucose, uric acid, and phosphorous measurements were within reference intervals.

After initial treatments and supportive care, survey radiographs were obtained the next day (day 2). Anesthesia was induced with 5% isoflurane in oxygen delivered by facemask, with the isoflurane levels decreased to the patient's requirements for maintenance. The survey radiograph obtained in lateral projection demonstrated increased soft tissue opacity and decreased small intestinal serosal detail in the caudal coelom. The ill-defined, amorphous soft tissue opaque structure was cranial to the renogonadal silhouette and partially summated on the caudal aspect of the lungs (Fig 1). Differential diagnoses for these findings were an airway-associated granuloma (fungal or bacterial) or neoplasm and coelomic fluid associated with coelomitis, hypoproteinemia, or neoplasia. The spleen appeared subjectively mildly enlarged (Fig 1). Differential diagnoses for splenic enlargement were splenitis (infectious/inflammatory), splenic congestion, and neoplasia.

For further evaluation, coelioscopy was performed on day 4. The bird was premedicated with midazolam (1 mg/kg IM) and butorphanol (1 mg/ kg IM, Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) before being induced with isoflurane, as previously described. After intubation with a 2-mm, uncuffed endotracheal tube, the bird was maintained on a nonrebreathing circuit and small-animal ventilator (Ventilator SAV, Vetronics, Lafayette, IN, USA), with the isoflurane adjusted to the patient's requirements. An intraosseous catheter was placed in the left ulna for fluid administration (lactated Ringer's solution. 10 mL/kg per h) and body temperature was maintained with an infant's portable, infrared warmer. The bird was placed in right lateral recumbency, and a standard coelioscopic examination was done with a 2.7-mm telescope system (Rigid Telescope 30[degrees], 2.7 mm with operating sheath, Karl Storz, Tuttlingen, BW, Germany). (2)

[FIGURE 2 OMITTED]

Endoscopic examination revealed hemorrhage within the caudoventral left lung, and a pale, granuloma-like structure within the caudal aspect of the left lung (Fig 2). Biopsies of the mass were collected with samples submitted for immediate intraoperative cytology and subsequent aerobic bacterial and fungal cultures. Intraoperative mod ified Wright's stained impression smears from the biopsy sample demonstrated well-differentiated epithelial cells associated with variable numbers of short, segmented, fungal hyphae or pseudohyphae, and globose, spore-like structures (Fig 3). A few scattered heterophils and mononuclear cells were also seen, configuring a mixed inflammatory response. Based on the cytologic results amphotericin B (1 mg/kg) was injected intralesionally with a 1.7-mm remote injection needle (Karl Storz).

After an uneventful recovery, treatment with itraconazole (10 mg/kg PO q12h, 30 days, Sporanox, Janssen Pharmaceuticals USA, Titusville, NJ, USA) and amphotericin B nebulization (1 mg/mF of saline for 15 minutes q8h for 2 days) was added to the treatment regime. Because culture results were still pending, the antifungal choice was made based on the most frequent cause of respiratory mycosis in birds, Aspergillus species. (3) By day 5, the bird was showing significant signs of improvement with increased appetite and a body weight of 132 g. Candida albicans was the only organism cultured from the biopsy.

[FIGURE 3 OMITTED]

On day 12, reevaluation of the complete blood cell count (CBC) indicated a significant increase in the leukocyte count to 152 000 cells/[micro]L, with a predominant heterophilia (133 700 cells/[micro]L), eosinophilia (1520 cells/[micro]L), lymphocytosis (9120 cells/[micro]L), and monocytosis (7600 cells/[micro]L). Despite patient improvement, there were concerns regarding drug resistance. Antifungal treatment was, therefore, changed to fluconazole (5 mg/kg PO, q12h) for 1 month, and the isolated Candida was submitted for antifungal susceptibility. The results indicated that the minimum inhibitory concentrations for fluconazole, itraconazole, and voricona zole were 0.125, 0.03, and 0.03 pg/mL, respectively. The owners declined to return the bird for a recheck examination; however, telephone communications documented that the bird continued to improve and was clinically normal by day 30. The bird has remained asymptomatic for 6 months since discontinuing all medications.

Discussion

This case report describes the clinical presentation, antemortem diagnosis, and successful treatment of pulmonary candidiasis in a sun conure. Candida species is a common environmental microorganism and a normal inhabitant of the avian digestive tract. It is an opportunistic avian pathogen usually restricted to the upper digestive tract, particularly the crop. (3) Secondary candidiasis is common and is usually associated with immune system suppression (eg, neonates, stress, overcrowding), concurrent disease (eg, hypovitaminosis A, malnutrition), prolonged broad-spectrum antibiotic therapy, or other causes of dysbiosis. (3,4) Although less frequent, primary candidiasis can occur. The prevalence of Candida species within the gastrointestinal tract of psittacine birds is common, but visceral and respiratory disease is rare. Conversely, Aspergillus species is a more frequent cause of respiratory mycosis in many companion, aviary, and free-ranging birds. (3)

Two reports describe the incidence of candidiasis, including disease associated with the respiratory system, in psittacine birds. In a report evaluating bacterial and mycotic isolates in psittacine birds, C albicans was isolated in 28 of 466 necropsy cases and 80 fecal samples. (5) Candidiasis was considered the primary infection in 5 of those cases, and all were related to the gastrointestinal tract. (5) In 4 lovebirds (Agapornis species), C albicans was cultured from yellow necrotic foci in the lungs, with epithelial metaplasia indicative of hypovitaminosis A in more than half of the cases. (5) This strengthens the argument that candidiasis is often associated with a compromised host defense. In a report describing necropsy results of 241 psittacine and passerine birds randomly collected from a pet bird farm, 31 (12.8%) of the birds had respiratory and integumental aspergillosis, and 37 (15.4%) had candidiasis involving the respiratory system, digestive tract, and/or skin. Candidiasis of the respiratory tract was mainly restricted to the nasal cavity (92%) and was more rarely associated with the larynx, trachea, and lung (12%). The authors associated the mycoses with predisposing factors, such as shipping and overcrowding. (6)

Atypical and respiratory candidiasis has also been reported in fowl and raptorial birds. A Candida tropicalis epidemic was described in a thousand turkeys secondary to antibiotic treatment. The birds were being supplemented with tetracycline, furazolidone, and chloramphenicol in the water and feed. Sixty-nine diseased birds had sinusitis, pneumonia, and air sac inflammation. Postmortem cytologic examination and culture of the affected organs identified C tropicalis. (7) Candida albicans and C tropicalis were isolated at necropsy from the respiratory tract of 2 chickens showing granulomatous nodular lesions. (8) Systemic candidiasis was described in a golden eagle (Aquila chrysaetos) with poxvirus infection, with C albicans cultured from the bird's lungs and cerebellum. A case of pulmonary infection by C albicans was reported in a goshawk (Accipiter species), whose hunting performance was deteriorated. The bird had no respiratory distress, but pulmonary rales were heard on auscultation. No radiographic evidence of lesions was seen, and the diagnosis was based on a positive reaction to C albicans antigen in a blood specimen. Treatment with oral itraconazole showed improvement and no reoccurrence of the clinical signs 5 months later. (9)

Candida albicans is frequently a secondary pathogen, and therefore, definitive diagnosis should be based on a culture of the specific agent in combination with histopathologic or cytologic demonstration of a pathologic host reaction. In our case, the clinical signs, inflammatory leukogram, and radiographic findings could be correlated to multiple causes, including Mycobacterium, Aspergillus, or Chlamydophila species infection. (10) Radiography identified nonspecific intracoelomic abnormalities, requiring that further diagnostic testing be performed. A definitive antemortem diagnosis and successful therapeutic plan were only made by endoscopic biopsy, cytologic examination, and culture. Achieving complete resolution of granulomatous disease can be difficult, especially because of the lesion's anatomic location. Surgical debridement and intralesional therapy have been advocated, with endoscopy representing a less invasive option. (3,11)

The bird improved clinically after initiating oral itraconazole and nebulization with amphotericin B. However, 1 week later, a repeat CBC demonstrated an increased leukocytosis with an increased heterophilia and monocytosis. Based on these hematologic results, and amid concerns of drug resistance, the treatment regime was changed from itraconazole to fluconazole. At that time, the isolated culture of C albicans was sent for susceptibility testing. The antifungal susceptibility results were obtained 20 days after beginning the fluconazole treatment. The results indicated that the isolated C albicans was susceptible to fluconazole, itraconazole, and voriconazole. Standard antifungal drugs, such as itraconazole, are not predictably effective against spore-forming fungi, such as Candida species, and that might explain the progression of the inflammatory leukogram. In retrospective, fluconazole would be preferred as initial antifungal therapy. Amphotericin B, itraconazole, and voriconazole are the first-line drugs for the treatment of mycelial yeast, such as Aspergillus species. (12)

The client elected not to return the bird for a recheck examination, but from telephone communications, the owners reported that the bird made a complete recovery and has remained clinically healthy for 6 months after discontinuing all medications. To the our knowledge, this is the first definitive antemortem diagnosis and successful treatment of pulmonary C albicans infection in an avian species. Although rare, pulmonary candidiasis should be on the list of differential diagnosis for any respiratory infection in birds.

Acknowledgments: We thank Supreme Pet Foods for supporting the UGA-Supreme Pet Foods Residency in Zoological Medicine and the UGA Sunshine fund for partially supporting the costs with the case.

References

(1.) Macwhirter P. Basic Anatomy, Physiology and Nutrition. In: Tully TN, Lawton MPC, Dorrestein GM, eds. Avian Medicine. Oxford, England: Butterworth-Heinemann; 2000:1-25.

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(3.) Bauck L. Mycoses. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers; 1994:997 1006.

(4.) Harcourt-Brown NH. Psittacine birds. In: Tully TN, Lawton MPC, Dorrestein GM, eds. Avian Medicine. Oxford, England: Butterworth-Heinemann; 2000:112-143.

(5.) Dorrestein GM, Buitelaar MN, van der Hage MH, Zwart P. Evaluation of a bacteriological and mycological examination of psittacine birds. Avian Dis. 1985;29(4):951-962.

(6.) Tsai SS, Park JH, Hirai K, Itakura C. Aspergillosis and candidiasis in psittacine and passeriforme birds with particular reference to nasal lesions. Avian Pathol. 1992;21(4):699-709.

(7.) Kuttin ES, Beemer AM, Bock RR, Perlstein Z. Candida tropicalis infecting the respiratory tract of turkeys in Israel. Avian Dis. 1975; 19(2):393-395.

(8.) Sharma VD, Sethi MS, Negi SK. Pulmonary candidiasis in fowl. Poult Sci. 1970;49(5): 1169-1171.

(9.) Boussarie D. A case of pulmonary mycosis in a goshawk: treatment with itraconazole. Action Vet. 1993;1245:13-14.

(10.) Fudge AM, Joseph V. Disorders of avian leukocytes. In: Fudge AM, ed. Laboratory Medicine: Avian and Exotic Pets. Philadelphia, PA: WB Saunders; 2000:19-27.

(11.) Hernandez-Divers SJ. Endosurgical debridement and diode laser ablation of lung and air sac granulomas in psittacine birds. J Avian Med Surg. 2002; 16(2): 138 145.

(12.) Chen SC, Playford EG, Sorrell TC. Antifungal therapy in invasive fungal infections. Curr Opin Pharmacol. 2010; 10(5):522-530.

Laila M. Proenga, DVM, MSc, PhD, Jorg Mayer, DVM, MS, Dipl ABVP, Dipl ECZM, Rodney Schnellbacher, DVM, Susan Sanchez, BSc, MSc, PhD, Chien-Tsun Huang, DVM, Holly Brown, DVM, PhD, David Jimenez, DVM, Dipl ACVR, Dainna Stelmach, DVM, and Stephen J. Divers, BVetMed, DZooMed, Dipl ACZM, Dipl ECZM, FRCVS

From the Departments of Small Animal Medicine and Surgery (Proensa, Mayer, Schnellbacher, Divers), Infectious Diseases (Sanchez), Veterinary Biosciences and Diagnostic Imaging (Jimenez, Stelmach), and Pathology (Huang, Brown), College of Veterinary Medicine, University of Georgia, 501 DW Brooks Dr, Athens, GA 30602, USA.
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Author:Proenca, Laila M.; Mayer, Jorg; Schnellbacher, Rodney; Sanchez, Susan; Huang, Chien-Tsun; Brown, Hol
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2014
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