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Peripheral nerve sheath tumor in a subadult golden eagle (Aquila chrysaetos).

Abstract: A 5-year-old, female golden eagle (Aquila chrysaetos) was admitted with tetraplegia that progressed to a nonambulatory, spastic tetraparesis after a few days of treatment. Clinical and radiologic examinations, including radiography, computed tomography scan, and myelography, were indicative of neoplasia involving a spinal nerve root. Postmortem magnetic resonance imaging and necropsy findings confirmed the diagnosis of a peripheral nerve sheath neoplasia, not, to our knowledge, previously reported in a raptor.

Key words: peripheral nerve sheath tumor, tetraplegia, nonambulatory, spastic tetraparesis, computed tomography scan, CT, myelography, magnetic resonance imaging, MRI, avian, golden eagle, Aquila chrysaetos

Clinical Report

A female, subadult golden eagle (Aquila chrysaetos) was presented because of lethargy and sternal recumbency to the Clinic for Zoo Animals, Exotic Pets, and Wildlife of the University of Zurich (Zurich, Switzerland). The animal had been found several days before, lying on the ground in a forest in the southern part of the Canton Ticino in Switzerland. The bird weighed 5.2 kg with subadult plumage, indicating an approximately 5-year-old bird. During clinical examination, the golden eagle was moderately depressed, slightly hypothermic, and tetraplegic. The animal had superficial skin wounds on several digits of both feet.

For diagnostic imaging, the bird was anesthetized with isoflurane, delivered by mask for induction, and immediately intubated. Survey radiographs and a computed tomography (CT) scan were done, and a blood sample was collected for a complete blood cell count (CBC) and plasma biochemical analysis. A fecal sample was submitted for parasitologic examination. On radiographs of the coelomic cavity, no abnormalities could be detected. Centered views of the extremities appeared unremarkable. On CT examination (Somaton Sensation Open, Siemens Medical Solution, Erlangen, Germany), the spinal cord had an even width and homogenous attenuation. The neuroforamen had an even width and shape. Foraminal fat could not be identified in any of the neuroforamen (Fig 1).

Results of hematologic testing showed a total white blood cell count of 22 700 cells/[micro]L (reference interval, 3200-32 100 cells/[micro]L) and a mild monocytosis of 1590 cells/[micro]L (reference interval, 950-1097 cells/[micro]L). (1) The biochemical analysis revealed a high concentration of aspartate aminotransferase (AST) (653 U/L; reference interval, 0-330 U/L) and creatine kinase (CK) (2948 U/L; reference interval, 183-937 U/L). (1) Fecal flotation results were negative. Treatment was started with Ringer's acetate and 5% dextrose given subcutaneously (calculated for 5% dehydration based on body weight), enrofloxacin (15 mg/kg SC q24h; Baytril 10%, Bayer Health Care, Provet AG, Lyssach, Switzerland), itraconazole (10 mg/kg PO q24h; Sporanox, Janssen-Cilag AG, Baar, Switzerland), vitamin B complex (30 mg/kg SC q24h), calcium disodium edetate (Ca-EDTA) (100 mg/kg SC q12h), and meloxicam (0.5 mg/kg SC q24h; Metacam, Boehringer Ingelheim (Schweiz) GmbH, Basel, Switzerland). Because of the possibility of osteomyelitis, clindamycin was added to the medical therapy 1 day later (100 mg/kg PO q24h, Antirobe, Pfizer AG, Zurich, Switzerland). Results of blood analysis of lead and zinc levels were negative, and treatment with Ca-EDTA was discontinued. Physical therapy was performed at least 2 times daily, and the eagle was force fed with beef and chicken meat, supplemented with vitamins. During the next several days, the bird improved slightly, moving both wings and legs. For a more comfortable position and to protect the feathers, the eagle was placed in a hammock (Fig 2), and the cloacal region was cleaned of feces and urates on a daily basis. Because no test for organophosphate toxicosis was readily available, a single dose of atropine (0.2 mg/kg IM) was given, but no clinical improvement was recognized.

A complete neurologic examination was performed after initial stabilization. During examination, the bird was bright and alert but remained in sternal recumbency and showed a nonambulatory, spastic tetraparesis. Results of cranial nerve tests were normal. Visual and tactile placing was absent, and the bird was not able to return the wings to a normal, folded position. The vent sphincter reflex, flexor reflex, leg and wing withdrawal reflex, sensory response of pelvic and thoracic limbs, and deep pain were present, but testing for superficial pain was questionable. Because of these findings, the lesion was assumed to be in the cranial cervical region.

The CBC and plasma biochemical analysis were repeated on days 7 and 11. No monocytosis was observed. The AST and CK concentrations remained above reference intervals but slowly decreased over time. On day 15, a survey radiographic and a myelographic study were performed to detect any abnormalities affecting the spinal cord. For this procedure, the bird was induced with isoflurane, intubated, and positioned in sternal recumbency. The results of the survey radiographs of the cervical spine were within reference range. A 3-cm region over the thoracolumbar spine was plucked of feathers and aseptically prepared, and a previously described myelographic injection technique was used. (2) Cerebrospinal fluid was visibly present in the spinal needle before contrast medium (Visipaque 270 mg/ mL, GE Health Care AG, Wadenswil, Switzerland) was injected. For injection, a 22-gauge spinal needle (0.7 x 38 mm, Terumo spinal needle, Terumo Corporation, Tokyo, Japan) was used. Approximately 0.5 mL of contrast media was injected over 1 minute, and additional contrast media was administered to achieve adequate contrast in the spinal column, as previously described. (2) In the lateral projection, the dorsal and ventral contrast columns were fading at the level of the intervertebral disk space C6/C7 (Fig 3). In the ventrodorsal and oblique projections, the contrast columns could not be identified. Because of the general lack of improvement and the overall poor prognosis, the golden eagle was euthanatized with a presumptive diagnosis of a mass, possibly neoplasia, involving a spinal nerve root. The carcass was submitted for a postmortem magnetic resonance imaging (MRI) immediately after euthanasia.

In the MRI examination (Achieva 3T, Philips AG, 8027 Zurich, Switzerland) of the spine, a small (4.5-mm diameter), tubular, space-occupying lesion was identified at the cervical intervertebral disk space 6/7 on the left side of the spinal cord. The lesion was mildly hyperintense in the fluid-sensitive MRI sequences and isointense in T1 in comparison to the spinal cord. The spinal cord was moderately displaced to the right side and moderately compressed. A "golf-tee"-sign could be identified in the transverse T2 weighted sequence. The space-occupying lesion extended through the left neuroforamen (Fig 4). The radiographic diagnosis was an intradural, extramedullary space-occupying lesion on the left side at the level of the intervertebral disk space C6/7. The lesion was highly suspicious for a peripheral nerve sheath tumor.

At necropsy, the eagle weighed 5.26 kg and was in a good body condition. Internal organs appeared normal, except the liver and kidneys, which were slightly swollen. On the left side, at the root of the spinal nerve between C6 and C7, an approximately 3x5 mm large mass was present. In this area, the corresponding nerve root was enlarged (Fig 5). Histologic examination of the spinal cord revealed an intradural but extramedullary, unencapsulated tumor located dorsally on the spinal cord, composed of loosely to sometimes densely arranged cells of ovoid to spindle shape, forming short, sometimes interwoven bundles, with indistinct cell borders and only slight eosinophilic cytoplasm. A moderate amount of fibrovascular stroma and slight pleomorphism and no mitotic figures were seen. On the edge of the tumor, swollen axons (spheroids) and Wallerian degeneration of the preexisting nerve could be seen. In the spinal cord, a large amount of swollen axons (spheroids) in all white matter funiculi as well as dilated myelin sheaths with myelinophages (digestion chambers) interpreted as Wallerian degeneration were found. In the gray matter, near the central canal and mostly dorsally, malacia with gitter cells and activated endothelial cells were present (Figs 6 and 7).

The liver and kidneys were hyperemic. A slight extramedullar hematopoiesis was found in the liver. The gizzard and the brain were without specific pathologic findings.

On immunohistochemical staining, the tumor was strongly positive for SI00, neuron-specific enolase, and vimentin and was weakly positive for glial fibrillary acidic protein stain (Table 1).

Based on the histologic features and immunohistochemical results, a peripheral nerve sheath tumor was diagnosed.

Discussion

In the present case, we describe a peripheral nerve sheath tumor at the level of the intervertebral disk space between C6 and C7 in a subadult, female golden eagle. The main neurologic sign during initial examination was tetraplegia, which progressed to a nonambulatory, spastic tetraparesis after a few days of treatment. Diagnostic imaging results, including radiographs, a CT scan, and myelography, were suspicious for neoplasia, involving a spinal nerve root. The postmortem MRI examination and necropsy confirmed that diagnosis.

Peripheral nerve sheath tumors (PNSTs) are neoplasms arising from Schwann cells, perineural cells, and intraneural fibroblasts. (3) Based on morphology and benignancy versus malignancy, they can be subdivided into schwannomas, neurofibromas, and malignant PNSTs. (4) Clinical signs can vary, depending on the location of the neoplasia.

Procedures to diagnose peripheral nerve neoplasms include radiography, CT scans, and MRIs. Myelography is necessary to evaluate the vertebral canal if a spinal nerve or nerve root neoplasia is suspected. (5) In small-animal medicine, the most common radiographic signs observed with nerve sheath neoplasm is the widening of an intervertebral foramen or remodeling around an enlarged nerve root, (5,6) but frequently, radiographs are normal. (5-7) Histologic examinations and immunohistochemistry can help to confirm the diagnosis of PNSTs.

With the exception of pituitary adenomas in budgerigars (Melopsittacus undulatus) and lymphosarcomas in chickens, neoplasias affecting the nervous system are only rarely described in birds. (8,9) Peripheral nervous system neoplasias include neurofibromas, neurofibrosarcomas, and lymphosarcomas. (8)

Neurofibromas have previously been reported in an adult green-winged macaw (Ara chloroptera). The animal was initially presented with a firm, submandibular, subcutaneous nodule and developed a second mass on the dorsal surface of the base of the tongue 3 weeks later. Histologic examination and peroxidase-antiperoxidase test confirmed the diagnosis. (10) In chickens, common sites of neurofibromas, neurofibrosarcomas, and neurogenic sarcomas are the skin, dorsal root ganglia, brachial plexus, brachial nerve, thoracic spinal ganglion, anterior mesenteric and celiac plexus, lumbosacral plexus, radial nerve, kidney, voluntary muscle, spleen, tongue, testis, and adrenal gland. (11) Observations on naturally occurring neoplasms in birds of Australia revealed one case of neurofibroma in a budgerigar with a nodular mass in the sciatic plexus with involvement of the adjacent kidney and one case of schwannoma in a peach-faced lovebird (Agapornis roseicollis) with a history of incoordination, loss of balance, and seizures. In the latter, a small nodule could be detected at the base of the brain stem, involving one of the cranial nerves. (12) Cases of multicentric neurofibrosarcoma have been previously described in Canada geese (Branta canadensis). (13,14)

As mentioned, no single, specific immunohistochemical marker is able to define PNSTs. (3) Therefore, a panel of different immunochemistry reagents was used in this case to further characterize the present neoplasia. The positive reaction for vimentin confirmed the mesenchymal origin of the tumor. That is consistent with findings in previous studies, in which PNSTs, being mesenchymal spindle cell tumors, were positive for vimentin in 100% of cases. (15,16) The positive reaction for neuron-specific enolase and SI00 both confirmed the neuronal origin of the tumor cells. Because SI00 identifies Schwann cells, consequently, most PNSTs express that molecule. (16) The weakly positive reaction for glial fibrillary acidic protein additionally supported the diagnosis of PNST.

In the eagle, we describe, clinical, radiographic, histologic, and immunochemical findings that confirmed the diagnosis of a peripheral nerve sheath neoplasia. To our knowledge, this is the first report of a peripheral nerve sheath tumor in a golden eagle and in raptors in general. Although peripheral nerve sheath neoplasias are uncommon in birds, they should be included in the differential diagnosis in any patient with neurologic signs.

Acknowledgments: We thank Marcus Clauss, the team of the Clinic for Zoo Animals, Exotic Pets and Wildlife, and the team of the Institute for Forensic Medicine, University of Zurich, for their assistance.

References

(1.) International Species Information System (ISIS) Web site, http://www.isis.org. Accessed May 2011.

(2.) Harr KE, Kollias GV II, Rendano V, deLahunta A. A myelographic technique for avian species. Vet Radiol Ultrasound. 1996:38(3): 187-192.

(3.) Hohsteter M, Smolec O, Gudan Kurilj A, et al. Intratesticular benign peripheral nerve sheath tumor in a ferret (Mustela putorius furo). J Small Anim Pract. 2012;53(1):63-66.

(4.) Schulmann FY, Johnson TO, Facemire PR, Fanburg-Smith JC. Feline peripheral nerve sheath tumors: histologic, immunohistochemical, and clinicopathologic correlation (59 tumors in 53 cats). Vet Pathol. 2009:46(6): 1166-1180.

(5.) LeCouteur RA, Withrow SJ. Tumors of the nervous system. In: Withrow SJ, Vail DM, eds. Withrow and MacEwen's Small Animal Clinical Oncology. 4th ed. St Louis, MO: Saunders Elsevier; 2007:659-685.

(6.) Bradley RL, Withrow SJ, Snyder SP. Nerve sheath tumors in the dog. J Am Anim Hosp Assoc. 1982;18:915-921.

(7.) Carmichael S, Griffiths IR. Tumours involving the brachial plexus in seven dogs. Vet Rec. 1981; 108(20):435-437.

(8.) Bennett RA. Neurology. In: Ritchie BW, Harrison GJ, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:728-747.

(9.) Jones MP, Orosz SE. Overview of avian neurology and neurological diseases. Semin Avian Exot Pet Med. 1996;5(3):150-164.

(10.) Bossart GD. Neurofibromas in a macaw (Ara chloroptera): morphologic and immunocytochemical diagnosis. Vet Pathol. 1983;20(6):773-776.

(11.) Campbell JG, Appleby EC. Tumours in young chickens bred for rapid body growth (broiler chickens): a study of 351 cases. J Pathol Bacteriol. 1966;92(1):77-90.

(12.) Reece RL. Observations on naturally occurring neoplasms in birds in the state of Victoria, Australia. Avian Pathol. 1992;21(1):3-32.

(13.) Siegfried LM. Neoplasms identified in free-flying birds. Avian Dis. 1983;27(1):86-99.

(14.) Locke LN. Multicentric neurofibrosarcoma in a Canada goose, Branta canadensis. Avian Dis. 1963;7(2): 196-202.

(15.) Bergmann W. Burgener I A, Roccabianca P, et al. Primary splenic peripheral nerve sheath tumour in a dog. J Comp Pathol. 2009;141(2-3):195-198.

(16.) Chijiwa K, Uchida K, Tateyama S. Immunohistochemical evaluation of canine peripheral nerve sheath tumors and other soft tissue sarcomas. Vet Pathol. 2004;41(4):307-318.

Morena Bernadette Wernick, Dr Med Vet, Dipl ECZM (Avian), Matthias Dennler, Dr Med Vet, Dipl ECVDL, Kathrin Beckmann, Dr Med Vet, Martina Schybli, Dr Med Vet, Sarah Albini, Dr Med Vet, Richard K. Hoop, Prof Dr Med Vet, Frank Steffen, PD, Dr Med Vet, Dipl ECVN, Patrick Kircher, Prof Dr Med Vet, PhD, Dipl ECVDI, and Jean-Michel Hatt, Prof Dr Med Vet, Dipl ACZM, Dipl ECZM (Avian)

From the Clinic for Zoo Animals, Exotic Pets and Wildlife (Wernick, Hatt), Section of Diagnostic Imaging (Dennler, Kircher), the Clinic for Small Animal Surgery/Neurology (Beckmann, Steffen), and the Department of Poultry and Rabbit Disease, Institute of Veterinary Bacteriology (Schybli, Albini, Hoop), Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

Table 1. Immunohistochemical results for antigen tests using vimentin,
neuron-specific enolase (NSE), SI00, and glial fibrillary acidic
protein (GFAP) in a 5-year-old, female golden eagle with tetraplegia.

Antibody used                     Specificity

Mouse anti-vimentin    Labels cells of mesenchymal
  (Dako M7020)           origin
Mouse anti-human NSE   Labels both normal and
  (Dako M087301)         neoplastic cells of neuronal
                         and neuroendocrine origin
Rabbit anti-SlOO       Labels both the [alpha] and [beta]
  (Dako N1573)           subunits of the human S100 protein
Rabbit anti-GFAP       Labels the intermediate
  (Dako N1506)           filament found in astrocytes
                         and some ependymal cells

Antibody used           Dilution            Method           Result (a)

Mouse anti-vimentin    1: 100       Detection (Dako K5003)   ++ to +++
  (Dako M7020)
Mouse anti-human NSE   1 : 150      Detection (Dako K5003)   +++
  (Dako M087301)
Rabbit anti-SlOO       Prediluted   Detection (Dako K5003)   +++
  (Dako N1573)
Rabbit anti-GFAP       Prediluted   Detection (Dako K5003)   +
  (Dako N1506)

(a) Results: + indicates slightly positive; ++, moderately positive;
+++ strongly positive.
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Title Annotation:Clinical Reports
Author:Wernick, Morena Bernadette; Dennler, Matthias; Beckmann, Kathrin; Schybli, Martina; Albini, Sarah; H
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2014
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