Overview of Tumors. Section II: A Retrospective Study of Case Submissions to a Specialty Diagnostic Service

Table of Contents

• Section I: Clinical Avian Neoplasia and Oncology
• Section II: A Retrospective Study of Case Submissions to a Specialty Diagnostic Service
• Neoplasia by Avian Order

• Psittaciformes
• Galliformes
• Anseriformes
• Passeriformes
• Phoenicopteridae
• Strigiformes
• Sphenisciformes
• Ciconiiformes
• Miscellaneous Orders

The occurrence of various types of avian neoplasia has been comprehensively reviewed [6]. This section documents the prevalence of neoplasms in 22 avian orders submitted to a specialty diagnostic service (Northwest ZooPath, Monroe, WA) from 1994 to 2002. Cases were selected based on histologic diagnosis. Cysts, hyperplastic processes, fibromatous polyps and poxvirus-related proliferative lesions were not included. Cases diagnosed as neoplastic based on cytology alone also were excluded. Although potentially reversible and not considered true neoplasms, adenomatous polyps and papillomas were included because of the known association of these lesions with concurrent neoplasia in psittacine birds [4]. Type, location, biological behavior and patient outcome are addressed. Apparent trends for particular types of neoplasms in some orders or species also are identified and discussed. For the purposes of this manuscript, prevalence refers to a given percentage within the study population, and the study population comprises the cases submitted to the service. The prevalence of these neoplasms in the populations from which these birds originated is not known.

Table 20.2.1 lists the tumor submissions by site and biological behavior. Skin was the most common site for tumor development, followed by alimentary tract, reproductive tract and liver. In all locations except alimentary tract, malignant tumors were more common than benign tumors; the large numbers of cloacal and oral papillomas and adenomatous polyps in psittacine birds account for this variation in behavior.

Table 20.2.2 summarizes total numbers of submissions and total numbers of tumors for each order. For the study period, 9574 avian samples were submitted, representing 22 orders; 557 neoplastic processes were identified, for an overall prevalence of 5.8%. The overall prevalence of neoplasia over the 7-year period was highest in Anseriformes (ducks, geese, swans), Galliformes (poultry, pheasants), Strigiformes (owls) and Cuculiformes (cuckoos, turacos).

Table 20.2.3 and Table 20.2.4 list the tumor submissions by type and biological behavior. The most common types of tumors were cutaneous squamous cell carcinoma, multicentric lymphoma, cutaneous soft tissue sarcoma, biliary adenocarcinoma and ovarian/oviduct adenocarcinoma.

Neoplasia by Avian Order

Psittaciformes

Order Psittaciformes (parrots and related species) had 3545 representatives and 220 neoplastic processes (prevalence = 6.2%) (see Table 20.2.2), slightly higher than the average prevalence for tumor submissions from other orders. Table 20.2.5 summarizes the most common presentations of neoplasms within this order. Trend criteria were based on total number of tumor types in a species (two or more), and percent of total for all tumors in a species (10% or greater). Using these criteria, numerous trends were observed within this order. For cockatiels (Nymphicus hollandicus), trends were identified in soft tissue sarcoma, squamous cell carcinoma, ovarian/ oviduct adenocarcinoma, fibrosarcoma and seminoma. For Amazon parrots (Amazona spp.), trends were identified for squamous cell carcinoma, cloacal adenomatous polyp, cloacal papilloma and biliary adenocarcinoma. For macaws (Ara spp.), trends were identified for cloacal adenomatous polyp, cloacal papilloma and biliary adenocarcinoma. For cockatoos (Cacatua spp.), trends were identified for soft tissue sarcomas and cloacal adenomatous polyps. For budgerigars (Melopsittacus undulatus), trends were identified for soft tissue sarcoma, squamous cell carcinoma, fibrosarcoma and renal adenocarcinoma. Interestingly, although lipomas are recognized as a common tumor in budgerigars [6,12], a trend was not identified in this analysis of submissions. This may be because clinicians easily recognize these tumors, thus biopsies are not routinely submitted. For lovebirds (Agapornis spp.), trends were identified for soft tissue sarcoma, fibrosarcoma and lymphoma. For African greys (Psittacus erithacus) and rosellas (Platycercus spp.), trends were identified for squamous cell carcinoma.

Cloacal Adenomatous Polyps and Papillomas

Cloacal adenomatous polyps were common in Amazon parrots and macaws, and also were seen in cockatoos (Cacatua spp.), an African grey, a thick-billed parrot (Rhynchopsitta pachyrhyncha) and a Patagonian conure (Cyanoliseus patagonus). This distribution is similar to that of retrospective studies of this condition [4,14]. Malignant transformation of cloacal "papillomas" has been described in psittacine birds [6,14]. In this study, four cloacal adenomatous polyps (two macaws, one amazon parrot and one cockatoo) underwent local transformation to adenocarcinoma, although no metastases were seen. Adenomatous polyps also were noted in the proventriculus of a cockatoo and on the eyelid of a cockatiel. Two cloacal adenomatous polyps were associated with concurrent biliary adenocarcinoma and two with concurrent pancreatic adenocarcinoma. Cloacal papillomas also were common in macaws and Amazon parrots, and one was seen in an African grey. Concurrent or isolated oral/choanal papillomas were occasionally seen. Only one of the cloacal papillomas was associated with concurrent biliary adenocarcinoma, and none were associated with malignant transformation in the cloaca.

Proliferative lesions of the cloacal mucosa of psittacine birds are well recognized [4,6,14]. Although typically referred to as papillomas, there are different morphologic presentations: a papilliform proliferation of squamous mucosal epithelial cells resembling a typical papilloma; and an adenomatous proliferation of glandular and villous mucosa more typical of a polyp, perhaps best termed an adenomatous polyp. Although the morphologic features of cloacal adenomatous polyps and papillomas differ, it is possible that these represent different morphologic variants of the same disease process. Both have similar site and species predilections, and both are sometimes associated with concurrent pancreatic and biliary malignancies. However, the distinction between cloacal adenomatous polyps and papillomas may not be purely academic. Based on this collection of the two cloacal phenotypes, the adenomatous polyps appear to have the most potential for undergoing malignant transformation in the cloaca, and for being associated with concurrent pancreatic or biliary neoplasia. Cloacal papillomas have been associated with herpesvirus gene sequences [5,13].

Bimorphic Pulmonary Neoplasms of Cockatiels

Four separate cases of an unusual malignant pulmonary neoplasm were seen in cockatiels. The birds presented with a history of dyspnea and usually had a radiographically apparent mass in the thoracic region of the coelomic cavity. Microscopically, the tumor involved the lung and spread by extension to serosal surfaces of viscera, especially heart and air sacs. One case of possible metastasis to the endocardial surface also was seen. The tumor appeared to arise within the pulmonary parenchyma, around the parabronchi. These neoplasms have unusual cell morphology and are characterized by densely cellular sheets of round to elongate cells with large vesicular to amphophilic smudged nuclei. The cells stain positively for mammalian vimentin, a mesenchymal cell marker, and have cytoplasmic intermediate filaments consistent with vimentin, suggesting that the cells are of mesenchymal origin. The cells stain negatively for mammalian epithelial pan cytokeratins; however, desmosomes, a feature of epithelial cells, are occasionally seen between adjacent cells. The cell of origin is poorly understood, but the tumors appear to be "bimorphic" with mesenchymal and epithelial cell components. The nuclear characteristics of the neoplastic cells resemble the inclusions caused by polyomavirus, but no virus has been detected by electron microscopy, in situ hybridization or PCR (M.M. Garner, unpublished data).

Galliformes

Order Galliformes (chickens, turkeys, pheasants, peafowl) had 783 representatives and 74 tumors (9.5%) (see Table 20.2.2), considerably higher than the average for tumor submissions from other orders. Table 20.2.6 summarizes the most common presentations of neoplasms within this order. Trend criteria were based on total number of a tumor type in a species (two or more), and percent of total for all tumors in a species (10% or greater). Using these criteria, numerous trends were observed within this order. For chickens, trends were identified for lymphoma, ovarian/oviduct adenocarcinoma and squamous cell carcinoma. These tumors are well recognized in poultry [2,10,11,16]. Some of these tumors, particularly the lymphoid malignancies, may have been associated with or induced by viral infection [2,10,11,16]. The only identifiable trend in pheasants was for interrenal cell adenoma, an otherwise uncommon tumor in birds. For guinea fowl, trends were identified for squamous cell carcinoma, seminoma and hepatocellular carcinoma. The only trend identified in peafowl was lymphoma. For turkeys, trends were identified for ovarian/oviduct adenocarcinoma and lymphoma. Herpesviruses and retroviruses have been identified as important causes of neoplasia in gallinaceous birds, particularly chickens and turkeys [2,10,11,16], and it is possible that viral oncogenesis was a factor in many of the cases within this order; however, serologic and other ancillary testing for viral causes was not routinely performed on case submissions, so viral status of affected birds was generally not known.

Anseriformes

Order Anseriformes (ducks, geese, swans) had 1024 representatives and 119 tumors (11.6%) (see Table 20.2.2), considerably higher than the average for tumor submissions from other orders. All the birds were adults or aged and most tumors likely occurred spontaneously. Trend criteria were based on total number of a tumor type in a species (two or more), and percent of total for all tumors in a species (10% or greater). Using these criteria, only two trends were identified: lymphoma and biliary adenocarcinoma in ducks, although a broad spectrum of neoplastic processes was represented in this group.

Passeriformes

Order Passeriformes (songbirds) had 1441 representatives and only 27 tumors (1.9%) (see Table 20.2.2), considerably below the average for other orders, suggesting that spontaneous neoplasia in passerine birds is relatively uncommon. All birds were adults, a broad spectrum of neoplastic processes was represented and tumors likely occurred spontaneously in most cases. One possible trend was observed: two mynahs had hepatic malignancies and concurrent hemochromatosis, suggesting iron storage in the liver may precipitate malignant transformation in this species, as alluded to by other authors [8,9].

Phoenicopteridae

Suborder Phoenicopteridae (flamingos) had 265 representatives and 13 tumors (4.9%) (see Table 20.2.2), suggesting that the overall prevalence of neoplasia in the family/suborder is about average. Interestingly, liver tumors accounted for slightly less than half of the tumor submissions (see Table 20.2.1), suggesting that hepatic neoplasia may be over-represented in captive flamingos. These birds typically store large amounts of iron in the liver [7,15] and all the flamingos with hepatic neoplasia in this study had iron deposition; however, no overt changes were noted morphologically in relation to the iron, such as cirrhosis seen in mynahs, toucans or birds of paradise [3,7,15] so the significance of the iron deposition relative to the neoplasia is undetermined. Two flamingos had squamous cell carcinomas on the pads of the feet, and had previous and ongoing protracted episodes of bumblefoot, which may have predisposed to neoplastic transformation.

Strigiformes

Order Strigiformes (owls) had 131 representatives and 13 tumors (9.9%) (see Table 20.2.2), suggesting that overall prevalence of neoplasia in this order may be relatively high compared to other orders in the study. Six of the owls were burrowing owls (Athene cunicularia), suggesting that these birds may have a higher than average prevalence of neoplasia. Three hepatocellular neoplasms were noted in this order, all in burrowing owls. Myelolipoma, an unusual neoplasm in birds, appears to be over-represented in owls, occurring in three cases in the study. All were intracoelomic neoplasms that were extensively invasive and of undetermined origin. Interestingly, the two affected snowy owls (Nyctea scandiaca) were pen mates for most of their lives and died from these tumors within months of each other. All three of the owls with myelolipomas were from the same zoo.

Sphenisciformes

Order Sphenisciformes (penguins) had 204 representatives and 11 tumors (5.4%) (see Table 20.2.2), about average compared to submissions from other avian orders. Over half of the tumor submissions (6, 55%) were squamous cell carcinomas, occurring in four different species of penguins. These data suggest that, in general, penguins may be predisposed to development of this form of neoplasm.

Ciconiiformes

Order Ciconiiformes (herons, storks, ibises, spoonbills, New World vultures) (see Table 20.2.2) had 307 representatives and 11 tumors (3.6%), indicating the overall incidence of neoplasia in this order was slightly below the submitted average. Eight of the tumor submissions were in roseate spoonbills (Ajaia ajaja) and seven of the tumors in this species were focal or multicentric renal adenomas, a tumor that was otherwise uncommonly encountered in avian submissions. These data indicate that roseate spoonbills may be predisposed to developing this form of neoplasia. Although benign, four of these tumors contributed directly to the cause of death.

Miscellaneous Orders

Several orders had no apparent trends in neoplastic disease. These include Columbiformes (pigeons, doves), Gruiformes (cranes, related species), Falconiformes (eagles, hawks, falcons, Old World vultures), Charadriiformes (shorebirds), Coraciiformes (kingfishers, mot mots, hornbills), Cuculiformes (turacos, cuckoos), Piciformes (woodpeckers, toucans, barbets), Struthioniformes (ratites), Coliiformes (mousebirds) and Pelecaniformes (pelicans, cormorants). Two birds of undetermined species also had neoplastic processes. Four orders, Gaviiformes (grebes, loons), Procellariiformes (fulmars), Caprimulgiformes (tawny frogmouths) and Apodiformes (hummingbirds) were represented in low numbers and had no neoplastic processes (see Table 20.2.2).