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History

A deceased juvenile (^4-month-old), female, scarlet macaw (Ara macao) was submitted to the Athens Diagnostic Laboratory at the University of Georgia, College of Veterinary Medicine, for postmortem examination. Several birds in this flock, including 2 other juvenile scarlet macaws, were affected by a "wasting syndrome," and 3 birds had died. The owner reported that this macaw had disseminated skin lesions for approximately 10 days and was previously treated for staphylococcal skin infection with trimethoprim-sulfamethoxazole per os at an unspecified dose, frequency, and duration.

Upon gross examination of the macaw, it had a body condition score of 2/5 and marked generalized feather loss. Multiple, variably sized, yellowish raised nodules were present on skin that was both feathered and unfeathered (Figs 1 and 2). Some nodules were ulcerated, whereas others had central depressions. Several white plaques were present on the oral mucosa around the choana, and yellow nodules were present on the tongue. The left lung and the caudal portion of the right lung were markedly congested and edematous, and fibrinous exudate was present on the pleura. The abdominal air sacs were opaque and thickened and covered with moderate amounts of fibrinous exudate. The liver was moderately enlarged and had a thickened capsule. The spleen and kidneys were pale. The crop was distended and filled with pasty food.

Diagnosis

Histopathologic evaluation of the skin nodules revealed marked hyperplasia of the epidermis with ballooning degeneration of cells and numerous eosinophilic intracytoplasmic inclusion bodies (Fig 3). In some areas, the epidermis was multifocally ulcerated and covered with a fibrinoheterophilic infiltrate with numerous yeasts and pseudohyphae consistent with Candida species as well as colonies of coccoid bacteria (Fig 4). A focal feather follicle had effaced feather follicle epithelium and was surrounded by a fibrinonecrotic exudate containing degenerated epithelial cells with eosinophilic intracytoplasmic inclusions. The underlying dermis had multifocal perivascular and interstitial infiltrates composed of lymphocytes and plasma cells (Fig 3).

The oral mucosa and tongue also had multifocal erosions and ulcerations of the epithelium, with degeneration and necrosis of superficial epithelial cells. Some degenerated cells had eosinophilic globular material in the cytoplasm resembling viral inclusions. In some areas, the mucosal epithelium was hyperkeratotic and covered with a fibrinonecrotic inflammatory infiltrate admixed with similar yeasts and pseudohyphae, colonies of coccoid- and rod-shaped bacteria, and plant material. The lung contained eosinophilic homogeneous material (edema) admixed with colonies of coccoid-shaped bacteria and plant material within parabronchi. Some air sacs had small granulomas and were also infiltrated with fibrin, lymphocytes, and plasma cells. There was moderate lymphoid depletion in the bursa of Fabricius and spleen. Some lymphoid follicles of the bursa were effaced by fibrinoheterophilic infiltration admixed with yeasts, pseudohyphae, and colonies of coccoid-shaped bacteria. Bacteriology results on lung samples revealed heavy growth of Klebsiella pneumoniae, and air sacs had heavy growth of Escherichia coli, Proteus species, and Enterococcus species. Fluorescent antibody testing for Chlamydia (Chlamydophila) psittaci was negative. The gross and microscopic lesions in the skin of this scarlet macaw are consistent with avian poxvirus infection and secondary candidiasis and bacterial infection.

Comments

Avian poxviruses are members of the genus Avipoxvirus of the Poxviridae family, which comprises a group of morphologically similar, large and complex DNA viruses that have varied degrees of host specificity. (1) Avian poxvirus is reported to occur in 3 forms, the wet or diphtheritic form, the dry or cutaneous form, and the systemic form. (1,2) The diphtheritic form is characterized by slightly elevated, opaque to white, fibrinonecrotic lesions on the mucous membranes of the oral cavity, esophagus, larynx, and trachea; this form tends to be associated with higher morbidity and mortality among pet birds and commercial poultry. (1,3) The dry or cutaneous form is characterized by proliferative lesions on the skin and may be the most common form diagnosed in avian species presented to veterinary hospitals. The disseminated form is highly fatal and occurs in canaries and finches. Avian pox can be diagnosed on the basis of clinical signs and laboratory findings, including cytology, histopathology, electron microscopy, virus isolation, polymerase chain reaction testing, and enzyme-linked immunosorbent assay. (1,3) Infection with avian poxvirus usually occurs by transmission of the virus through compromised surface epithelium by direct contact with infected birds or mechanically, by insect vectors or contaminated objects. (1,3) Lesions of the cutaneous form include papules, pustules, and nodules usually located on the unfeathered areas of the body, particularly, on the eyelids, cere, legs, and feet. (4) This case is unusual because the pox lesions were present not only on unfeathered skin but also under feathered areas. The skin lesions were often associated with fungal organisms consistent with Candida species and coccoid-shaped bacteria, which were likely Staphylococcus species. Multifocal ulcerative lesions were identified on the oral mucosa and tongue from which fungal organisms consistent with Candida species were seen, as well as rod- and coccoid-shaped bacteria. Degenerated epithelial cells with eosinophilic globular material resembling viral inclusions were observed in tissue collected from the tongue, suggesting that this macaw also had the diphtheritic form of avian pox. The fibrinoheterophilic pneumonia and airsacculitis admixed with plant material is consistent with aspiration, which may have been caused by difficulty swallowing because of obstructive and painful lesions in the oral cavity and tongue.

Avian pox appears to be a rare condition in psittacine birds located in the United States and primarily causes ocular or upper digestive tract lesions in affected birds. (5) Few cases of atypical cutaneous pox involving feathered areas in commercial broilers have been reported, and the lesions in these cases were associated with skin scratches. (6,7) There is also one report of cutaneous pox involving feather follicles around the uropygial glands in mynah birds (.Acridotheres cristatellus). (8) In the present case, the stress of the disease and weight loss may have affected the ability of this bird to recover from infection, resulting in alopecia and disseminated cutaneous lesions. The immunocompromised state of this bird due to lymphoid depletion likely predisposed the patient to secondary candidiasis and bacterial infection.

There is no specific treatment for avian pox. Antiseptic solutions and antibiotic and antifungal therapy may be recommended to treat secondary infections. Control of pox infection can also be attained by appropriate disinfection of equipment and premises, with affected birds being separated from the flock to prevent the transmission of the virus through scabs. Sanitation with appropriate disinfectants is recommended because the avian poxvirus can persist in dried scabs within the birds' environment for months. (3) Arthropod vectors should also be controlled, because infections are generally more prevalent when mosquito vectors are present. Another preventative measure is raising birds in cages equipped with protective screens to prevent the entry of mosquitoes. (1)

In conclusion, this case helps to remind clinicians that avian pox should be included on the list of differential disease diagnoses of birds with any multifocal proliferative lesions on the skin. Additionally, cutaneous pox lesions are often infected by commensal bacterial and fungal organisms, which may increase the difficulty of diagnosing the primary viral disease.

This case was submitted by Carmen Jerry, DVM, Raquel R. Rech, DVM, MS, PhD, Dipl ACVP, and Monique S. Franga, DVM, PhD, Dipl ACPV, Dipl ACVP, from the Department of Pathology, University of Georgia, Athens, GA, USA (Jerry); the Department of Veterinary Pathobiology, Texas A&M University, College Station, TX 77843, USA (Rech); and the Poultry Diagnostic and Research Center, Department of Population Health. University of Georgia, Athens, GA 30602, USA (Franga).

Please review the clinical history, gross necropsy findings, and Figures 1 and 2, then formulate a list of differential diagnoses before continuing.

References

(1.) Ritchie BW. Poxviridae. In: Ritchie BW, ed. Avian Viruses: Function and Control. Lake Worth, FL: Wingers Publishing Inc; 1997:285-311.

(2.) Phalen DN. Viruses. In: Altman RB, Clubb SL, Dorrestein GM, Quesenberry K, eds. Avian Medicine and Surgery. Philadelphia, PA: WB Saunders; 1997:281-322.

(3.) Tripathy DN. Reed WM. Pox. In: Saif YM. Fadly AM, Glisson JR, et al, eds. Diseases of Poultry. 12th ed. Ames, IA: Blackwell; 2008:291-307.

(4.) Schmidt RE, Reavil DR. Phalen DN. Integument. In: Schmidt RE. Reavil DR. Phalen DN, eds. Pathology of Pet and Aviary Birds. Ames, IA: Blackwell; 2003:184.

(5.) Shivaprasad HL, Franca M. Unusual disseminated lesions of poxvirus in psittacines resembling canary pox. Proc Anna Conf Assoc Avian Vet. 2011:275-276.

(6.) Senties-Cue CG, Charlton BR. Woolcock P, et al. Atypical distribution of fowl pox lesions in broilers. Avian Dis. 2010;54(4): 1316-1318.

(7.) Back A, Sonconi RA, Ruthes O, et al. An atypical fowl pox outbreak in broilers in southern Brazil. Avian Dis. 1995;39(4):902 906.

(8.) Hsieh YC, Chen SH, Wang CW, et al. Unusual pox lesions found in Chinese jungle mynahs (Acridotheres cristatellus). Avian Pathol. 2005;34(5):415-417.
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Title Annotation:postmortem examination of a scarlet macaw
Author:Jerry, Carmen; Rech, Raquel R.; Franga, Monique S.
Publication:Journal of Avian Medicine and Surgery
Geographic Code:1USA
Date:Sep 1, 2015
Words:1456
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