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Keywords:

  • avian;
  • eyelid;
  • globe;
  • lymphoma;
  • neoplasia;
  • ocular

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Ocular and eyelid lesions are a common finding in birds; however, avian ocular and eyelid neoplasia is seldom reported. The purpose of this study was to record clinical and pathological data from cases of avian ocular neoplasia submitted to the Comparative Ocular Pathology Laboratory of Wisconsin over a 29-year period. A total of 284 avian ocular pathology cases from 1982 to 2011 were reviewed. Out of those, 15 were diagnosed with nine different ocular tumors (5.2%). Metastatic cancer to the globe was diagnosed in seven cases. Six of the metastatic cancers were diagnosed as lymphoma and one as papillary cystic carcinoma of respiratory epithelial origin, presumably originating in the sinus. Primary tumors were diagnosed in eight cases including three tumors of epithelial origin (undifferentiated carcinoma, multicystic adenoma, and pigmented iridociliary adenoma). A teratoid medulloepithelioma and a ganglioneuroma were presumptively diagnosed. A round cell tumor and squamous cell carcinoma were detected in conjunctival samples, and a teratoma was diagnosed from an episcleral sample.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Ocular and eyelid lesions are a common finding in birds;[1] however, there are few reports of avian ocular and eyelid neoplasia in the literature. A variety of benign and malignant tumors have been reported, both primary and metastatic, affecting the eye, including medulloepitheliomas,[2, 3] lymphoreticular tumors,[4] melanocytic tumors,[5, 6] and rhabdomyosarcomas.[7] Several retrobulbar and eyelid tumors have also been reported, including a retrobulbar adenocarcinoma,[7] a glioma,[8] a liposarcoma,[9] and two mast cell tumors.[10, 11] The authors are unaware of published data regarding the prevalence of ocular neoplasia in birds to date.

The ocular anatomy of birds is similar to that of mammals; however, there are a number of differences that may impact oncogenesis and the clinical signs observed in affected animals. A notable difference is the presence of 10–18 ossicles and hyaline cartilage within the sclera, both of which support the eye.[12, 13] The iris and ciliary body muscles are striated, in contrast to mammals, allowing voluntary contraction and dilation of the pupil.[12] In a number of species, including Passeriformes, falcons, and woodpeckers, a U-shaped bone (os opticum) is embedded in the scleral cartilage around the optic nerve.[13] In some species, the infraorbital sinus is connected with pneumatized sections of the skull bones which spread toward the more dorsal and rostral parts of the beak, jaw, and orbit.[12]

The purpose of this study is to document cases of ocular neoplasia together with relevant clinical information from Comparative Ocular Pathology Laboratory of Wisconsin (COPLOW) over a 29-year period.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Two hundred and eighty-four avian ocular pathology submissions from 1982 to 2011 were reviewed in order to select cases of ocular neoplasia. Original submission forms, pathology reports, and histology slides were reviewed. The following information was collected when available: age, sex, location of the neoplasm, existence of metastatic lesions, ophthalmic finding, physical findings and source of the animal/sample. All samples were submitted immersion fixed in 10% neutral buffered formalin. The specimens were decalcified when necessary, transected, routinely processed, embedded in paraffin, and sectioned at 5 μm. Sections were stained with hematoxylin and eosin and examined by light microscopy.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

Fifteen cases (5.2%) from 284 submissions were diagnosed with nine different neoplasms affecting the globe, eyelids, or retrobulbar space (Table 1). Biopsy (9/15) or necropsy (4/15) specimens were received from birds kept as pets (9/15), from commercial sources (1/15) or zoological collections (2/15) (Table 1). In two cases (2/15), it was unknown whether samples were acquired from biopsy or necropsy, and in three cases, there was no information regarding the source of the birds (Table 1). The age was known in 9/15 cases, ranging from 7 months (case 13) to 35 years (case 14). The gender was known in nine cases, with six males and three females documented (Table 1).

Table 1. Ocular and eyelid neoplasia in birds submitted to Comparative Ocular Pathology Laboratory of Wisconsin (1982–2011)
Case #SpeciesAgeSexLocationSampleDiagnosisSourceClinical signsOther tissues affected
  1. U = unknown; F = female; M = male; y = year; and m = month.

1Chicken (Gallus domesticus)UUUULymphomaUUU
2Cockatoo (Fam. Cacatuidae)5 yFUpper eyelidBiopsyRound cell tumorPetNoneNo
3Chicken (Gallus domesticus)UUGlobeBiopsyGanglioneuromaUUU
4ParakeetUUOrbitNecropsyMetastatic papillary cystic carcinomaPetUnilateral exophthalmosRetrobulbar space bilaterally, cervical area
5Peacock (Pavo spp.)4.5 yMOrbitULymphomaPetBuphthalmia, lethargy and anorexia for 1 mGlobe and extraocular tissues
6Peacock (Pavo spp.)4 yMOrbitNecropsyLymphomaPetLethargy for the past 3 daysMultiple tissues
7African grey parrot (Psittacus erithacus)UMGlobeBiopsyTeratoid medulloepitheliomaPetNoneNo
8Peacock (Pavo spp.)6 yFOrbitNecropsyLymphomaUOrbital swelling for 1 weekMultiple tissues
9Turkey (Meleagridis spp.)16 yUEpiscleraBiopsyTeratomaCommercialMass on the eyeNo
10Dove (Zenaida macrouraUMOrbitBiopsyUndifferentiated carcinoma (DDx amelanotic melanoma)Pet2 week history of exophthalmia, inappetence and weight loss. Left head tiltU
11African grey parrot (Psittacus erithacus)27 yMConjunctivaBiopsySquamous cell carcinomaPet2 month history of periorbital swelling and caseous dischargeN
12Sun conure (Aratinga solstitialis)3 yUGlobeBiopsyLymphomaPetNoneU
13Tragopan (Tragopan spp.)7 mUGlobeNecropsyLymphomaZooBlind and depressedMultiple tissues
14Great indian hornbill (Buceros bicornis)35 yFGlobeBiopsyMulticystic adenomaZooSmall globe, keratitis and conjunctivitisN
15Yellow-crested cockatoo (Cacatua sulphurea)UMGlobeBiopsyPigmented iridociliary adenomaPetNoneNo

Metastatic neoplasms

Metastatic neoplasia of the eye was diagnosed in seven cases (cases 1, 4, 5, 6, 8, 12, and 13).

Lymphoma was diagnosed from six cases (cases 1, 5, 6, 8, 12, and 13), and one case was diagnosed as a papillary cystic carcinoma of respiratory epithelial origin (case 4). The ophthalmic and clinical findings prior to the biopsy/necropsy were known in six cases (cases 4, 5, 6, 8, 12, and 13). In all of these cases, animals presented with ocular or general clinical signs, such as exophthalmia/buphthalmia (cases 4 and 5), orbital swelling (case 8), or blindness (case 13), and a degree of depression and/or lethargy was noted in three of five cases (cases 5, 6, and 13).

Lymphoma

Histologically, lymphoma cases (Fig. 1a–d) were characterized by sheets of neoplastic round cells morphologically consistent with lymphocytes, which infiltrated, expanded, and often effaced the uvea. Neoplastic cells infiltrated the sclera, peripheral cornea, and extended into the orbit in all of these cases. Immunohistochemical stains were not performed. Reticuloendotheliosis virus (REV) DNA proviral sequences were detected from polymerase chain reaction (PCR) testing of frozen samples of liver and spleen from case 5.[14] No further testing was performed in the other cases.

image

Figure 1. Lymphoma in different species (H&E). Lymphoma in tragopan (case 13) (a), chicken (case 1) (b), sun conure (case 12) (c), and peacock (case 8) (d). (a) The uvea is diffusely infiltrated and effaced with a population of neoplastic round cells. The neoplastic infiltrate extends into the sclera in the limbal area (arrow) and around the optic nerve head (arrow head). (b) A population of neoplastic round cells multifocally infiltrates the anterior uveal stroma (arrows). (c) The globe is markedly distorted. The uvea is diffusely and unevenly infiltrated and effaced by a population of neoplastic lymphocytes. (d) A population of neoplastic cells expands and effaces the choroid and extends into the sclera. The retina is multifocally detached (arrow).

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Metastatic papillary cystic carcinoma

A single case of this tumor was observed in a parakeet (case 4). The retrobulbar space was infiltrated and obscured with cuboidal and occasionally ciliated neoplastic cells, which were arranged in ductal and papillary infoldings (Fig. 2a–b) separated by variable amounts of fibrovascular stroma. Neoplastic cells infiltrated the orbit and extended into cervical connective tissue, with multifocal areas of cranial bone destruction. The globes were bilaterally intact. No immunohistochemical stains were performed.

image

Figure 2. Metastatic cystic adenocarcinoma in a parakeet (H&E). (a) Neoplastic epithelial cells are arranged in cords and often form cystic spaces. (b) Neoplastic cells are polygonal to cuboidal, with indistinct cell borders, have moderate amounts of eosinophilic cytoplasm and an oval nucleus with often indistinct nucleoli.

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Primary neoplasms

Primary ocular or eyelid tumors were diagnosed in eight birds (cases 2, 3, 7, 9, 10, 11, 14, and 15). Specimens from these eight cases included five globes, one episcleral sample and two conjunctival samples. Clinical history was provided in seven of eight cases with primary neoplasia. All presented with ophthalmic signs; however, only one bird showed systemic disease (case 10). This animal presented with weight loss, anorexia, and head tilt (Table 1).

Globes/orbit

Of the five globes, three had tumors of epithelial origin (undifferentiated carcinoma, multicystic adenoma, and pigmented iridociliary adenoma) and two presumptive diagnoses of a teratoid medulloepithelioma and ganglioneuroma were made.

An undifferentiated carcinoma was diagnosed in a dove (case 10). The left eye and fragments of tissue from the orbit were submitted for the examination. Histologically, most of the uvea, retina, and vitreous were effaced by a neoplastic infiltrate that extended through the sclera. Neoplastic cells were arranged in dense sheets and nests and separated by fine fibrovascular stroma. Cellular pleomorphism was marked and mitotic figures were frequent. Differential diagnosis included amelanotic melanoma. Periodic acidic–Schiff (PAS) stains revealed irregular staining of basement membranes, and a diagnosis of epithelial tumor was favored; however, immunohistochemical stains were not performed. In this case, given the extent of the neoplastic infiltrate and the clinical signs displayed by the animal, the possibility of this being a metastatic tumor was entertained; however, this could not be confirmed.

A multicystic adenoma was diagnosed in a Great Indian hornbill (case 14). The uvea and retina were replaced, and the globe was filled with a population of columnar to tall cuboidal neoplastic epithelial cells arranged in cystic structures and trabeculae. Cellular pleomorphism was mild and mitotic figures were infrequent. Multifocal, stromal mucin accumulation was noted, and intracytoplasmic mucin was observed in some neoplastic cells. Neoplastic epithelial cells showed no immunoreactivity for vimentin, cytokeratin, or synaptophysin.

A pigmented iridociliary adenoma was diagnosed in a yellow-crested cockatoo (case 15). Histologically, a well delineated, nonencapsulated mass expanded the uvea and filled 60% of the globe. The mass was composed of interconnected trabeculae of pigmented epithelial cells separated by a fibrovascular stroma with prominent blood vessels. Neoplastic cells often contained pigment granules in their cytoplasm. Cellular pleomorphism was mild, and mitotic figures were infrequent.

A presumptive teratoid medulloepithelioma was diagnosed in an African grey parrot (case 7). A space occupying mass composed of a population of pleomorphic neoplastic cells extended from the iris. The neoplastic cells were elongated to round, with moderate to large amounts of clear, pale amphophilic cytoplasm, and pleomorphic nuclei showing frequent cytoplasmic invaginations. Occasional large nucleoli were noted. Some of the neoplastic cells showed cytoplasmic cross-banding, suggestive of skeletal muscle differentiation. Neoplastic cells showed immunoreactivity for neuron-specific enolase (NSE), desmin, and glial fibrillary acidic protein (GFAP). Ambiguous immunoreactivity for S-100 was noted. Immunoreactivity was not observed with CD-57 or vimentin stains.

A presumptive ganglioneuroma distorted the posterior aspect of the globe in a chicken (case 3). The mass extended through the sclera into the choroid where it affected up to three-quarters of the posterior aspect of the globe, and infiltrated rostrally through the choroid effacing one side of the ciliary body and iris. The mass was composed of interwoven spindle cells with scattered cells morphologically consistent with ganglion cells (Fig. 3a–b). No immunohistochemical stains were performed.

image

Figure 3. Ganglioneuroma in a chicken (case 3) (H&E). (a) A mass distorts the posterior aspect of the globe. The mass extends through the sclera into the choroid over approximately three-quarters of the posterior aspect of the globe (★). The mass infiltrates rostrally through the choroid and extends within the globe on one side of the ciliary body and iris (arrowhead). The retina is diffusely detached (arrow). (b) The mass is composed of interwoven spindle cells with intermittent ganglion cells (arrow).

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Conjunctiva

A round cell tumor (case 2) and a squamous cell carcinoma (case 11) were diagnosed from conjunctival samples. In case 2, neoplastic cells resembled plasma cells; however, no immunohistochemical stains were performed.

Episclera

A teratoma was diagnosed from episcleral tissue (case 9). Histologically, the mass was characterized by the presence of the three primordial germ cell lines with foci of brain-like tissue (ectoderm), cartilage, bone, smooth muscle and fibrous connective tissue (mesoderm), and respiratory epithelium (endoderm).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The purpose of this study was to record clinical and pathological data from cases of avian ocular and eyelid neoplasia submitted to the COPLOW over a 29-year period. Of the 284 cases in our collection, only 15 were ocular tumors (5.2%). The prevalence of ocular disease in birds has been reported to be 7.6% and between 14–26% in birds of prey;[12] however, to the best of the author's knowledge, there are no data regarding prevalence of ocular tumors in birds. Avian ocular neoplasia can necessitate euthanasia in production animals or require medical and surgical treatment in companion and zoo animals. Vision is a primary sensory pathway for birds,[15] and any mass affecting the globe, orbit, or eyelids can interfere with vision. The resulting ocular lesion in a wild bird can lead to starvation and death, whereas an ocular lesion in captive birds can become a welfare problem.

The ages documented in our review ranged from 7 months (case 13) to 35 years (case 15). The youngest age reported in the literature is an 8-week-old commercial chicken with an ocular rhabdomyosarcoma[7] and the oldest a great horned owl aged 31 years with an iridal melanoma.[5] The gender was known in 9 of our cases, with six males and three females. Given the difficulty in determining the gender in many of the avian species, it is rarely recorded in the literature.

The ophthalmic findings varied with the anatomic locations of the tumors; however, when the information was provided, many of the animals presented with some clinical ocular signs. Exophthalmos is regularly observed with space occupying masses in the retrobulbar area, as seen in several of our cases. In the few cases in the literature with clinical information, common findings were as follows: no discernible clinical signs,[3, 4, 16, 17] poor body condition, weakness, and/or dehydration.[2, 4, 18-20] Of our eight cases of primary globe, eyelid, or orbit tumors, only one bird (case 10) showed inappetence and weakness. A history was not provided in one other case, and no other physical findings, such as depression or inappetence, were noted in the remaining six cases. In our cases of metastatic tumors to the globe, three presented with signs such as depression or anorexia (cases 5, 6, and 13) and a history was not provided in one of the cases.

Reticuloendotheliosis virus (REV) DNA was detected by PCR from one of our cases of lymphoma.[14] The etiology of lymphoma in birds, other than for few commercial species, is unknown.

Ocular medulloepithelioma is an embryonal tumor from the primitive neuroectodermal tissue primarily seen in young animals and children, although these tumors are also rarely reported in adult humans.[21-23] In our case, the age of the African grey parrot was not known. Intraocular medulloepitheliomas have also been reported in cockatiels,[2, 3] and in these cases, the birds were 1 year and 11 months old.

These types of tumors characteristically arise from the nonpigmented epithelium of the ciliary body. Medulloepithelioma also arises from the iris, retina, or optic disk.[23] These tumors range from benign proliferations to malignant neoplasms with invasive capacity; however, they exhibit limited metastatic potential. Some medulloepitheliomas are composed purely of primitive neuroepithelial cells (nonteratoid medulloepithelioma), whereas others develop a teratoid component characterized by differentiation of tissues from at least one other germ line (such as cartilage or striated muscle). In our case, neoplastic cells showed immunoreactivity for neuron-specific enolase (NSE), desmin, and glial fibrillary acidic protein (GFAP), immunoreactivity for S-100 was not assessable due to nonspecific and background staining, and immunoreactivity with CD-57 or vimentin stains was not observed. The immunohistochemical stain results and the presence of a few areas of skeletal muscle differentiation suggested a diagnosis of teratoid medulloepithelioma.

Immunohistochemical stains on tissue from our cystic adenoma case (case 14) did not show immunoreactivity for vimentin, cytokeratin, or synaptophysin. However, given that no studies currently exist regarding immunohistochemical characteristics in normal avian ocular tissues, little significance can be drawn from this result.

The conjunctival squamous cell carcinoma diagnosed in the African grey parrot (case 11) exhibited common characteristics of similar tumors described in other species. One case of squamous cell carcinoma in the third eyelid of a conure exists in the literature.[24] Squamous cell carcinomas occur relatively frequently in the sunlight-exposed, nonpigmented epithelium of the eyelids, bulbar conjunctiva, and third eyelid of cattle living outdoors in sunny environments.[25] There is not enough information to correlate this neoplasm with sunlight exposure.

Ganglioneuromas are rare neuroblastic tumors of the peripheral nervous system that originate mainly from the cranial and spinal ganglia.[21, 22] These tumors are rarely observed in domestic animals. Histologically, they present as a mixture of both poorly differentiated and well-differentiated ganglion cells, found singly or in clusters, admixed with closely packed streams of spindle cells and nerve fascicles. In our case, the presence of relatively well-differentiated ganglion cells suggested the diagnosis of ganglioneuroma. Reports of ganglioneuromas in birds are scarce in the literature.[26]

Birds have upper and lower eyelid plus a nictitating membrane. Tumors are frequently reported in the eyelid and third eyelid of birds;[18, 23, 27] however, only one of our cases of neoplasia originated from this area (case 2). In this case, the mass had been progressing for 2.5 years. No other signs were reported. Histologically, neoplastic cells resembled well-differentiated plasma cells; however, immunohistochemistry was not performed.

In summary, ocular lesions are relatively common in birds; however, the prevalence of ocular tumors in birds is not well known as reports on ocular neoplasms in birds are relatively scarce in the literature. The aim of this paper was to document avian ocular neoplasms received at COPLOW over the last 29 years in order to add cases with relevant clinical information to the literature. Immunohistochemistry is an important tool in the diagnosis of tumors in domestic animals; however, little is known regarding normal immunoreactivity of ocular tissues in birds. This represents a vital area of potential further study in the effort to establish accurate prognostic and prevalence data of ocular tumors in birds.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References

The authors would like to thank Stephen D. Cahalan, and Stephanie M. Bostic for their editorial assistance.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgment
  8. References
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