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Title: Case Study: Feline spinal cord gemistocytic astrocytoma

Authors: Elisângela Olegário da Silva; Raquel Beneton Ferioli; Kleber Moreno; Ana Paula F.R.L.

ID: 29645-2011

 


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4.REPORT: This case report will aid in the diagnosis of this rare condition in the cat. The report is generally well written and histopathological findings support the diagnosis. There is extensive information concerning the condition in other species in the Introduction and the Discussion which may be superfluous in this case. It would be useful to provide maybe a similar differential with image. In text change “In feline” to In felines. Accept with minor changes see attached revised manuscript below.

ABSTRACT

Primary spinal cord tumors are rare in cats. A six-year-old, intact male Siamese cat had a history of progressive hemiparesia, muscle atrophy in the right thoracic limb and pain in that region. Neurological examination revealed increased reflexes, hyperesthesia and propioceptive deficit in the right thoracic limb. Medical therapy was initiated, but neurological signs were progressive and severe, affecting the pelvic limbs. The owner opted for euthanasia. Gross exam showed a swollen area in the C6 region of the spinal cord. Histopathological examination showed diffuse proliferation of large cells with abundant eosinophilic cytoplasm and eccentrically located large nuclei with prominent 8positive staining for S100, vimentin and GFAP (glial fibrillar acid protein) and negative staining for macrophage antigens (lysozyme and LN-5). Based on histopathological and immunohistochemical features, the diagnosis of gemistocytic astrocytoma was made.

INTRODUCTION

Neoplasias of the central nervous system (CNS) can be neuroectodermal, mesodermal or of nervous root origin (Jones, 2006). Gliomas are the most common type of tumor of neuroectodermal origin in humans (Rasheed and Bigner, 1997, Gavin et al., 2002) and animals (Koestner and Higgins, 2002). Astrocytomas comprise the majority of canine gliomas but are uncommon in feline (Summers et al., 1995). Astrocytomas occur most commonly in the pyriform lobe, convexity of the cerebral hemisphere, thalamus and hypothalamus, and in the midbrain, but they are rarely found in the cerebellum and spinal cord (Storts, 1995; Koestner and Higgins, 2002).

In felines, primary tumors of the CNS are uncommon (Fondevila et al., 1998), but meningiomas and lymphomas are the most frequent when found (Zaki and Hurvitz, 1976; Parker et al., 1983). There are two reports of primary spinal cord gemistocytic astrocytoma in felines (Aloisio et al., 2008; Marioni-Henry et al., 2008), and this is the first case  report from South America.

Gemistocytic astrocytomas are variants of diffuse astrocytomas characterized by the presence of gemistocytic astrocytes (Martins et al., 2001; Avninder et al., 2006). The gemistocytes are characterized by abundant, glassy eosinophilic cytoplasm and eccentrically placed nuclei. These cells are not present in normal tissue or during embryogenesis of the CNS (Kros et al., 1991; Avninder et al., 2006).

According to the WHO’s classification system for humans, gemistocytic astrocytomas are characterized by the presence of a conspicuous, though variable, fraction of gemistocytic astrocytes and are classified as grade II (Kleihues et al., 2002), but the percentage of gemistocytic cells necessary to classify a gemistocytic astrocytoma as a tumor is not specified. Some reports propose that at least 20% of gemistocytic astrocytes should be present in a human CNS tumor to classify it as a gemistocytic astrocytoma (Krouwer et al., 1991; Avninder et al., 2006). In the veterinary literature, no reports about the use of the gemistocytic index to classify a tumor as gemistocytic astrocytoma were found because was no used it so far.

The definitive diagnosis of a spinal cord tumor can be achieved only after histopathological analysis (LeCouteur and Grandy, 2005), and the immunohistochemical assay has become an indispensable technique for confirmatory diagnosis (Koestner and Higgins, 2002). This report is important since it describes the clinical, radiological, pathological and immunohistochemical findings associated with this tumor in a cat; comparative aspects in human beings are also discussed.

CASE REPORT

A six-year-old, intact male Siamese cat was admitted to the Veterinary Hospital, Universidade Estadual de Londrina, Londrina/PR, Southern Brazil. The animal had a history of progressive hemiparesis, muscle atrophy in the right thoracic limb and pain in this region for approximately five weeks. Clinical and neurological examinations led to the diagnosis of spinal cord dysfunction. Increased reflexes, hyperesthesia and propioceptive deficit were observed in the right thoracic limb. Plain radiography was performed, with no alteration. Medical therapy was initiated, but neurological signs were progressive and severe, affecting the pelvic limbs, which showed increased reflexes, propioceptive deficit and spastic paresis. Seven days after the initial examination, the owner opted for euthanasia. Routine necropsy was performed soon after death; selected tissues (brain, spinal cord, lung, kidneys, liver, heart, and spleen) were fixed in 10% buffered formalin solution and routinely processed for histopathological evaluation. Sections were stained with hematoxylin-eosin (HE) and periodic acid Schiff (PAS). The gemistocytic index was quantified by counting 200 cells in five different fields under 40x magnification and calculating the average number of gemistocytic cells.

Selected paraffin-embedded tissue fragments from the spinal cord were prepared for immunohistochemical (IHC) analysis. Immunostaining was performed using a polymer-based detection kit. Slides were incubated with one of five primary antibodies: GFAP, vimentin, macrophage antigens (lysozyme and LN-5) or S100 protein. For IHC, the polymer-peroxidase technique was used. Antibody dilution and incubation time followed the manufacturer’s recommendations. The color reaction to detect the antigen was carried out with 3,39-diaminobenzidine. Tissue fragments from nervous tissue, lymph nodes, and breast were used as positive controls; for negative controls, mouse serum substituted the primary antibody.

Gross examination showed a intramedullary swollen area in the C6 region of the spinal cord. After fixation, the spinal cord was cut, revealing a well-delimited, whitish and soft area in the right lateral region of the C6 segment (Figure 1). The affected region comprises the lateral funiculus. The histopathology exam showed diffuse proliferation of large cells with distinct borders, abundant eosinophilic cytoplasm and eccentrically located large nuclei with prominent nucleoli (Figure  2, 3, 4). Glial fibers were scarce, atypia was moderate and mitotic index was low. The average gemistocytic index was 72.2%. The PAS method showed no staining of the granules within the cytoplasm of neoplastic cells. The immunohistochemical assay showed positive GFAP  (Figure 5), staining for S100 and  vimentin (Figure 6) and negative staining for lysozyme and LN-5 (macrophage) was showed in table 1. Based on histopathological and immunohistochemical features , the diagnosis of gemistocytic astrocytoma was made.

DISCUSSION

Tumors of the central nervous system are common in humans and constitute the second most prevalent type of tumor in childhood (Wilson et al., 2002). Glial tumors are among the most common primary tumors of the central nervous system in humans (Rasheed and Bigner, 1997; Balmaceda et al., 2002), dogs and cats (Koestner and Higgins, 2002).

 Astrocytoma is the most common glial tumor in canines (Maxie and Youssef, 2007) and is most frequently diagnosed in brachycephalic breeds, such as Boston Terriers and Boxers ( S’antana et al., 2002), with greater incidence in animals over five years of age (Storts 1995; Stoica et al., 2004; Zachary, 2007). In the cat, astrocytomas are uncommon and when discovered, are most frequent in cats over nine years of age (Santana et al., 2002; Henry et al., 2008).  Some reports demonstrate that the occurrence of astrocytomas in dogs and cats can be related to genetic alterations such as inactivation of p53 and overexpression of EGFRP (Stoica et al., 2004; Stoica et al., 2009).

The spinal cord can be invaded or compressed by primary or metastatic neoplasias arising from the vertebral column and surrounding structures. Primary neural tumors include ependymoma, glioma, neurofibroma, neurofibrosarcoma, schwannoma, meningioma, meningeal sarcoma, neuroepithelioma, reticulum cell sarcoma and astrocytoma (LeCouteur and Grandy, 2005).

In children, spinal cord tumors represent 1-10% of all tumors of the central nervous system (Wilson et al., 2007), and intramedullar spinal cord astrocytomas represent 6-8% of all spinal cord tumors (Minehan et al., 2008). In animals, intramedullar neoplasia of the spinal cord is less common than the extramedullar form (DeLahunta, 1983). In general, extradural, intradural-extramedullar and intramedullar tumors cannot be distinguished on the basis of clinical signs (Luttgen et al., 1980; DeLahunta, 1983, LeCouteur and Grandy, 2005). Intramedullar tumors are reported to cause a more rapid progression of clinical signs and to be much less likely to be painful than extradural or intradural-extramedullary tumors (LeCouteur and Grandy, 2005).

The clinical signs depend on the location of the tumor in the spinal cord and also on whether more than one segment is involved. Compressive lesions within the cervical portion of the vertebral canal often cause cervical hyperesthesia and minimal or no neurological deficits because of the relatively larger diameter of the cervical portion of the vertebral canal compared with the diameters of the thoracic and lumbar regions. Intramedullar spinal cord tumors, such as astrocytomas, usually hasten neurological dysfunction (LeCouteur and Withrow, 2007) and are less amenable to surgical removal (DeLahunta, 1983).   The cat showed neurological signs compatible with a lesion of an upper motor neuron (DeLahunta, 1983), such as progressive muscle atrophy from disuse, increased reflexes, hyperesthesia and propioceptive deficits. The tumor did not affect the nerve root because the cat did not show signs of lower motor neuron lesion. The tumor had a continuous progression, and the meninges were compressed, causing painful increased sensitivity in the right thoracic limb.

The complementary techniques used to confirm the presence of neoplasia in the spinal cord are plain radiography, cerebrospinal fluid analysis (CSF), myelography and specialized radiographic techniques such as computerized tomography and magnetic resonance imaging (Parker et al., 1983; Wheeler et al., 1985; LeCouteur and Grandy, 2005). Plain radiography did not show evidence of intramedullary spinal tumor (Wright et al., 1979; Fenner, 1994), but myelography may be helpful in differentiating intramedullar, intradural-extramedullar and extradural neoplasia (LeCouteur and Grandy, 2005). In this case, no alteration was evidenced on plain radiography. Due to the cat’s rapid progression of clinical signs and increased pain, the owner opted for euthanasia, and no further imaging examination was performed.

A definitive diagnosis of nervous tumors is possible through only histopathological examination. However, immunohistochemical assay has become an indispensable technique to confirm diagnosis and to classify nervous system tumors (Barnhart et al., 2002; Koestner and Higgins, 2002). The histopathological classification of the CNS tumors in animals is primarily based on cell type, pathological behavior, topographic pattern and secondary changes present within and surrounding the tumor (LeCouteur and Withrow, 2007).

The presence of gemistocytic astrocytes in CNS tumors is considered a marker of poor prognosis, as these cells are not present in normal tissue. However, their role remains unknown. The gemistocytic index in this case was 72.2%, far higher than the percentage found in the human gemistocytic astrocytoma (Krouwer et al., 1991; Avninder et al., 2006). This value demonstrates that gemistocytic astrocytoma can be more aggressive in cats than in humans. Gemistocytic astrocytoma exhibits a tendency toward aggressive clinical behavior due to its increased propensity for recurrence and rapid progression to glioblastoma (Burton and Prados, 2000; Aloisio et al., 2008).

An important differential diagnosis is granular cell astrocytoma, which shows histological findings similar to gemistocytic astrocytoma. Large round to oval cells with distinct borders and abundant eosinophilic granular cytoplasm characterize granular cell astrocytoma (Higgins et al., 2001; Shi and Morgenstern, 2008).  PAS staining can be used to demonstrate the presence of granules within the cytoplasm. In this case, the tumor was negative for PAS staining. Positive staining for S100 protein and vimentin and negative staining for GFAP were reported in granular cell tumors (Higgins et al., 2001; Mandara et al., 2006). The immunohistochemical procedure was performed using antibodies against lysozyme and LN-5 to rule out a tumor of monocyte/histiocyte phenotype. On the other hand, the positive immunostaining for S100, vimentin and GFAP indicated that the tumor had an astrocytic derivation. The histological and immunohistochemical findings are in accordance with the characteristics described in the literature for gemistocytic astrocytoma (Summers et al., 1995; Avninder  et al., 2006; Baena et al., 2007).

The prognosis of animals with tumors of the CNS depends on tumor location, surgical accessibility, growth and degree of damage to the nervous system (DeLahunta, 1983). The prognosis for  feline with intramedullary spinal cord astrocytoma is poor, as this condition has a relentlessly progressive course (Fenner, 1994; Jeffery and Phillips, 1995). Clinical signs and laboratory and imaging exams generally do not yield conclusive diagnoses. Histopathological and immunohistochemical methods are fundamental for the definitive diagnosis and classification of intramedullary spinal cord tumors.

In conclusion, gemistocytic astrocytoma was diagnosed and confirmed in this cat due to the characteristic histopathological and immunohistochemical findings that are consistent with this neoplasia. This report contains information that would be useful to assist pathologist and veterinarians in the diagnosis and understanding of this uncommon disease entity in feline.

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