Cloacal Papillomas in Psittacine Birds: A Retrospective Histopathologic Review

Nancy L. Stedman, Kenneth S. Latimer, and Pauline M. Rakich

Department of Pathology (Stedman, Latimer) and Athens Diagnostic Laboratory (Rakich), College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602 (USA)

Abstract. A retrospective study of cloacal papillomas of psittacine birds was performed on tissue specimens submitted from 1993-1998. Cloacal papillomas occurred most frequently in Amazon parrots, macaws, and cockatoos. There was no apparent gender predisposition to papilloma development. The median age of affected birds was 4.5 years. The major clinical sign was "cloacal prolapse. " Most cloacal papillomas had a transitional to columnar epithelium and had a lower mitotic index than papillomas covered by squamous epithelium. Lymphoplasmacytic infiltrates were observed most commonly within these papillomas. One macaw had a concurrent oral papilloma, an unspecified breed of parrot had concurrent bile duct carcinoma of the liver, and an Amazon parrot had moderate to severe bile duct hyperplasia.

Key Words: Avian, Psittacine, Cloacal papilloma, Epithelium, Histopathology, Inflammatory cell infiltrates, Mitotic index, Concurrent neoplasia, Oral papilloma, Bile duct carcinoma, Bile duct hyperplasia

Introduction

Benign papillomas of the gastrointestinal tract develop commonly in psittacine birds, with cloacal involvement found most frequently at clinical presentation. ^2,5,12 The microscopic appearance of cloacal papillomas has been described as frond-like projections of proliferating epithelium on a fibrovascular stroma. ^2,10,12 The proliferating epithelium varies from stratified squamous to columnar with goblet cells. Mitoses frequently are seen within or near the basal layer. Heterophilic and lymphoplasmacytic inflammation is often present. In one case, herpesvirus-like inclusions were described, but typically microscopic evidence of viral infection is not observed. ⁴

This retrospective review summarizes the signalment, medical history, and histologic characteristics of cloacal papillomas from several psittacine species.

Materials and Methods

Case record and tissue selection: Case accession records from the Department of Pathology and the Athens Diagnostic Laboratory were reviewed for a five-year period (1993-1998) to identify diagnoses of "cloacal papilloma. " These records included both surgical biopsy and necropsy reports. Information related to gender and medical history were tabulated where available. Hematoxylin and eosin stained sections of formalin-fixed, paraffin embedded cloacal tissues subsequently were retrieved from archival storage for microscopic review, histologic classification, and lesion scoring.

Study population: Sections of biopsy and necropsy specimens from 34 psittacine birds with a diagnosis of cloacal papillomatosis were reviewed. These birds included 15 parrots: 4 Yellow-naped Amazon Parrots (Amazona ochrocephala ochrocephala), 3 unspecified Amazon Parrots (Amazona sp. ), 2 African Grey Parrots (Psittacus erithacus), 1 Blue-fronted Amazon Parrot (Amazona aestiva aestiva), 1 Mealy Amazon Parrot (Amazona farinosa), 1 Orange-winged Amazon Parrot (Amazona amazonica), 1 Yellow-crowned Amazon Parrot (Amazona ochrocephala oratrix), and 2 parrots of undetermined species; 10 macaws: 5 Blue & Gold [Yellow] Macaws (Ara ararauna), 2 Green-winged Macaws (Ara chloroptera), 2 macaws of undetermined species, and 1 Severe [Chestnut-fronted] Macaw (Ara severa); 5 cockatoos: 2 Moluccan [Salmon-crested] Cockatoos (Cacatua moluccensis), 2 Umbrella [White] Cockatoos (Cacatua alba), and 1 cockatoo of unspecified species; 3 conures: 1 Peach-fronted Conure (Aratinga aurea), 1 Red-masked Conure (Aratinga erythrogenys), and 1 conure of unspecified species; and 1 Alexandrine Parakeet (Psittacula eupatria).

Microscopic evaluation of cloacal papillomas: Epithelial type, mitotic index, and type and degree of inflammation were determined. Epithelial type was classified as columnar, squamous, or transitional depending on the predominant cell type. Transitional epithelium was defined as stratified epithelium with areas of adjacent squamous and columnar morphology, with neither predominating in the papilloma. The mitotic index was defined as the total number of mitotic figures present in ten random high power (45x) fields of view of papilloma epithelium. Inflammation was categorized by cell type, distribution, and severity. Additional features, such as ulceration, goblet cell hyperplasia, and keratinization, also were noted. Other tumors were noted if present; however, this information was not available for most biopsy specimens.

Results

A summary of the signalment data is given in Table 1. Twenty four cases (70.6%) of cloacal papilloma occurred in New World psittacines. Cloacal papillomas occurred most commonly in Amazon parrots, followed by macaws and cockatoos. The gender was given for 22 of 34 birds; 10 (45.5%) were male and 12 (54.5%) were female. Age was recorded for 16 of 34 birds. The mean age of affected birds was 6 years (range, 7 weeks to 17 years). The median age of affected birds was 4.5 years.

A medical history was included for 28 of the 34 birds. Exposed cloacal tissue, sometimes designated "cloacal prolapse," was observed in 22 of the birds (78.6%). In six of these birds (27.3%), the problem was described as recurrent. In two cases, straining was the presenting complaint. One male Moluccan cockatoo had a history of self-mutilation of the vent region. Reproductive problems were noted in two female psittacines. One female Moluccan cockatoo had a history of egg binding, while a female Peach-headed conure had a history of passing a large blood covered egg.

Eight papillomas (23.5%) had predominantly squamous epithelium. In one papilloma in a Red masked conure, the squamous epithelium was keratinized. Eleven papillomas (32.4%) had predominantly columnar epithelium. Fifteen papillomas (44%) had both types of epithelium and were classified as transitional. The epithelium in these cloacal papillomas often transitioned from columnar to squamous randomly throughout the papilloma (Fig. 1). Associations were not noted between any type of psittacine species and type of epithelium. In the Moluccan cockatoo with the history of egg binding, the columnar epithelium was also ciliated (Fig. 2).

Fig. 1. Moluccan Cockatoo, Female, Cloacal papilloma, H&E stain. Ciliated columnar epithelium covers the surface of the neoplasm.	Fig. 2. Yellow-naped Amazon Parrot, Cloacal papilloma, H&E stain. Both columnar and squamous epithelium are present upon the same frond.

The mean mitotic index for papillomas with squamous epithelium was 14.1, with a range of zero to fifty. The mean mitotic index for papillomas with columnar epithelium was 5.9, with a range of zero to 31. The latter case with a mitotic index of 31 was from a 17-year-old Blue and gold macaw. Of the papillomas with columnar epithelium, only this mass had a mitotic index greater than ten. Mitoses also were present within the superficial layers of the epithelium and were not confined to the basal layer. The mean mitotic index for papillomas with transitional epithelium was 5.2, with a range of zero to sixteen. In general, papillomas with squamous epithelium had more frequent mitoses than papillomas with either columnar or transitional epithelium (Fig. 3).

Fig. 3. Green-winged Macaw, Cloacal papilloma, H&E stain. The stratified squamous epithelium contains frequent mitoses.

A lymphoplasmacytic infiltrate was present in 30 of 34 papillomas (88.2%). In twenty nine of these papillomas, the infiltrate was mild and distributed multifocally within the superficial fibrovascular stroma adjacent to the basal cell layer. In one papilloma, a mild lichenoid plasma cell infiltrate was present adjacent to the squamous epithelium (Fig. 4). Heterophils were observed in 21 of the papillomas (61.8%). Heterophil distribution was similar to that described for lymphoplasmacytic infiltrates. In some cloacal papillomas, mild heterophil transmigration of the epithelium was observed (Fig. 5). In one cloacal papilloma from a macaw of unspecified species, a severe heterophilic infiltrate was associated with pustule formation in the transitional epithelium. Goblet cell hyperplasia was present in nine of the thirty four papillomas (26.5%). Focal to multifocal ulceration was present in only three cloacal papillomas (8.8%).

Fig. 4. Blue & gold Macaw, Cloacal papilloma, H&E stain. A mild lichenoid plasma cell infiltrate is present adjacent to the epithelium.	Fig. 5. Peach-headed Conure, Cloacal papilloma, H&E stain. Several heterophils are present transmigrating the epithelium of the mass. The fibrovascular stroma also contains several plasma cells.

One Green-winged macaw with cloacal papillomatosis also had a concurrent oral papilloma. A concurrent bile duct carcinoma was present in a 10-year-old male parrot of unspecified species with a cloacal papilloma. A male 6-year-old Amazon parrot of unspecified species with a cloacal papilloma also had moderate to severe bile duct hyperplasia.

Discussion

Signalment data from this study is consistent with previous reports that indicate cloacal papillomatosis is more frequently seen in New World psittacines. ^5,10,12 Although other reports have indicated that females may be more frequently affected than males, this study did not find a dramatic difference in gender distribution of cloacal papillomas. ^5,12 However, gender was unknown for 12 of the 34 cases. The mean and median ages of affected birds are similar to those given in other reports. ^5,12

The type of epithelium present in the normal cloacal mucosa varies with the organ chamber and species. The coprodeum and urodeum are lined by columnar epithelium with goblet cells in most species, but the proctodeal lining may vary from columnar to stratified squamous epithelium. ^1,3,9,11 The vent is lined by stratified squamous epithelium. ⁹ The variation in epithelial cell type in the cloacal papillomas reviewed for this study may reflect differing sites of origin within the cloaca. The presence of squamous and transitional epithelium in the majority of cases reflects clinical observations that cloacal papillomas commonly arise at or near the mucocutaneous junction adjacent to the vent. Papillomas with columnar epithelium and prominent goblet cell hyperplasia may arise more cranially within the cloaca. The origin of the papilloma with the ciliated columnar lining in the Moluccan cockatoo hen is unknown. Since the oviduct has a ciliated epithelial lining, this papilloma may have originated in the urodeum at or near this opening.

The etiology of cloacal papillomatosis remains obscure. DNA in situ hybridization, in situ polymerase chain reaction, and nested polymerase chain reaction failed to detect parrot papillomavirus nucleic acid in 24 cloacal papillomas and 2 oral papillomas. In one African grey parrot, however, all three techniques detected parrot papillomavirus in an oral papilloma. ¹⁰ Papillomavirus also was observed by transmission electron microscopy and detected by immunohistochemical staining in another African grey parrot with external papillomas on the face, suggesting a possible viral etiology for some papillomas in this species. ⁷ The presence of lymphoplasmacytic infiltrates in almost all cases examined suggests some consistent underlying antigenic stimulation. The degree of heterophil infiltration may reflect other factors such as secondary bacterial overgrowth and trauma.

Only two cases in this study had other concurrent neoplasms. Bile duct and pancreatic carcinomas previously have been associated with cloacal papillomas in psittacine birds. ^5,6,8 In our study, 19 of 34 cloacal papillomas were sampled by surgical biopsy. Therefore, the presence or absence of concurrent neoplasia remains unknown.

References

1. Calhoun M L: Microscopic Anatomy of the Digestive System of the Chicken. Ames, Iowa State University Press, 1954.

2. Cooper JE, Lawton MPC, Greenwood AG: Papillomas in psittacine birds. Vet Rec 119:535, 1986.

3. Dahm HH, et. al. : Scanning and transmission electron microscopic observations of the cloacal epithelia of the domestic fowl. Cell Tissue Res 211:83-93, 1980.

4. Goodwin MA, McGee ED: Herpes-like virus associated with a cloacal papilloma in an orange fronted conure. J Assoc Avian Vet 7:23-25, 1993.

5. Graham DL: Internal papillomatous disease - a pathologist’s view. Proc Assoc Avian Vet,Chicago, IL, 1991, pp. 141-143.

6. Hillyer EV, Moroff S, Hoefer H, Quesenberry KE: Bile duct carcinoma in two out of ten Amazon parrots with cloacal papillomas. J Assoc Avian Vet 5:91-95, 1991.

7. Jacobson ER, et. al. : Papilloma-like virus in an African grey parrot. J Am Vet Med Assoc 183:1307-1308, 1983.

8. Kennedy FA, Sattler-Augustun S, Mahler JR, Jansson PC: Oropharyngeal and cloacal papillomas in two macaws (Ara spp. ) with neoplasia with hepatic metastasis. J Av Med Surg 10:89-95, 1996.

9. King AS: Cloaca and vent. In: King AS McLelland J (eds): Birds: Their Structure and Function. Philadelphia, Balliere Tindall, 1984, pp. 187-199.

10. Latimer KS, et. al. : Investigation of parrot papillomavirus in cloacal and oral papillomas of psittacine birds. Vet Clin Pathol 26:158-163, 1997.

11. Pokras MA, Zupke K: Normal exfoliative cytology of the avian cloaca. J Assoc Avian Vet 5:77-82, 1991.

12. Sundberg JP, et. al. : Cloacal papillomas in psittacines. Am J Vet Res 47:928-932, 1986.

This Page Last Updated May 15, 1998

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