Accepted Manuscript Atypical Teratoid Rhabdoid Tumor in a Teenager with Unusual Infiltration Into the Jugular Foramen Yoko T. Udaka, MD, Janet M. Yoon, MD, Denise M. Malicki, MD PhD, Paritosh C. Khanna, MD, Michael L. Levy, MD PhD, John R. Crawford, MD MS PII:

S1878-8750(15)00881-5

DOI:

10.1016/j.wneu.2015.07.015

Reference:

WNEU 3042

To appear in:

World Neurosurgery

Received Date: 4 May 2015 Revised Date:

6 July 2015

Accepted Date: 8 July 2015

Please cite this article as: Udaka YT, Yoon JM, Malicki DM, Khanna PC, Levy ML, Crawford JR, Atypical Teratoid Rhabdoid Tumor in a Teenager with Unusual Infiltration Into the Jugular Foramen, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.07.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Highlights We describe the first case of ATRT invading the jugular foramen



ATRTs can have atypical presentations and radiographic features



ATRT should be included in the differential of tumors invading the jugular foramen

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Atypical Teratoid Rhabdoid Tumor in a Teenager with Unusual Infiltration Into the Jugular Foramen

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Yoko T Udaka MDa, Janet M Yoon MDa, Denise M Malicki MD PhDb, Paritosh C Khanna MDc, Michael L Levy MD PhDd, and John R Crawford MD MSa e

Department of Pediatrics Division of Hematology-Oncology, University of California, San Diego,

Rady Children’s Hospital-San Diego, San Diego, California, USA b

Department of Pathology, Rady Children’s Hospital-San Diego, San Diego, California, USA

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Department of Radiology, Rady Children’s Hospital-San Diego, San Diego, California, USA

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Department of Neurosurgery, Rady Children’s Hospital-San Diego, San Diego, California, USA

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USA

Corresponding Author Yoko Tina Udaka MD Department of Pediatrics Division of Hematology-Oncology

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University of California San Diego

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Department of Neurosciences, Rady Children’s Hospital-San Diego, San Diego, California,

Rady Children’s Hospital San Diego 3020 Children’s Way MC5035 San Diego CA 92123 Phone: +1 858 966-5811

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Fax: +1 858 966-8035

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Email: [email protected]

Key words: atypical teratoid rhabdoid tumor, jugular foramen, neuroimaging Abbreviations: ATRT: atypical teratoid rhabdoid tumor CNS: central nervous system CT: computed tomography DWI: diffusion weighted imaging ELITE: extreme lateral infrajugular transcondylar PNET: primary neuroectodermal tumor MRI: magnetic resonance imaging SEER: Surveillance, Epidemiology, and End Results WHO: World Health Organization

ACCEPTED MANUSCRIPT Udaka Abstract Background Atypical teratoid rhabdoid tumor is a rare malignant neoplasm that represents 1-2% of all

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pediatric central nervous system tumors. Immunohistochemistry plays an important role in establishing the diagnosis with a loss of INI-1 staining in tumor cells. In this case report we describe a teenager with an unusual presentation and pattern of infiltration of the tumor.

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Case Description

A 13-year-old boy presented with a several month history of progressive nausea, weight loss

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and hoarseness of voice associated with multiple lower cranial nerve palsies on neurologic examination. Magnetic resonance imaging revealed a large heterogeneously enhancing extraaxial neoplasm with extension and bony expansion of the jugular foramen. Following near total resection, neuropathology demonstrated absence of INI-1 expression consistent with a diagnosis of atypical teratoid rhabdoid tumor.

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Conclusions

This case highlights the diverse clinical presentation and infiltrative potential of atypical teratoid

jugular foramen.

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Key words:

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rhabdoid tumors, thus expanding the differential diagnosis of extra axial tumors invading the

atypical teratoid rhabdoid tumor, jugular foramen, neuroimaging Abbreviations: ATRT: atypical teratoid rhabdoid tumor CNS: central nervous system CT: computed tomography DWI: diffusion weighted imaging ELITE: extreme lateral infrajugular transcondylar PNET: primary neuroectodermal tumor MRI: magnetic resonance imaging SEER: Surveillance, Epidemiology, and End Results WHO: World Health Organization

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Introduction Primary childhood brain and central nervous system (CNS) tumors occur at an incidence of 5.1 per 100,000 person-years and are the most common solid tumor of childhood. (9) Atypical

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teratoid rhabdoid tumor (ATRT) is a rare malignant neoplasm that represents 1-2 % of all pediatric CNS tumors but comprises 10-20% of CNS tumors in children less than 3 years of age. (3, 12) ATRTs are highly aggressive tumors with up to 20% of patients showing

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disseminated disease at the time of presentation. (14) ATRTs were previously classified as medulloblastoma or primary neuroectodermal tumors (PNETs) until described as a separate

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entity in the 1980s, and now the World Health Organization (WHO) classifies ATRT as a distinct tumor type. (17, 24) Consequently, it is thought that the actual number of cases of ATRT has been significantly underestimated in the past. (4, 27) Immunohistochemistry plays a pivotal role in the diagnosis of ATRT with an observed loss of INI-1 staining in tumor cells and preservation in normal surrounding tissue. (10) The authors report a case of a teenage boy who presented

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with a several month history of multiple lower cranial nerve palsies, found to have a large extraaxial tumor infiltrating the jugular foramen on neuroimaging for which pathology revealed an ATRT. This case illustrates an unusual pattern of ATRT infiltration into the jugular foramen and

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the neurosurgical challenges of such unique malignant tumor extension.

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Case Report History and Examination A 13-year-old previously healthy boy presented to the hospital following a 4-6 month history of

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progressive nausea and vomiting, a 22 pound weight loss, and hoarseness of voice. These symptoms were preceded by a 2-year history of frequent throat clearing that was thought to be a motor tic. His neurologic examination at presentation revealed multiple lower cranial nerve

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palsies including asymmetric palatal elevation with deviation of the uvula to the left, decreased gag, hypophonic voice, rightward tongue deviation, right-sided dysmetria, and mild left

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hemiparesis. Computed tomography (CT) with contrast demonstrated a heterogeneously enhancing extra-axial cerebellopontine angle mass with extension into the right jugular foramen and extensive bony remodeling (Figure 1A-B). Magnetic resonance imaging (MRI) of the brain confirmed a large right-sided extra-axial mass with reduced diffusivity on diffusion weighted imaging (DWI) sequences with invasion of the jugular foramen (Figure 1C). More linear central

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hypointense areas visualized within the jugular foramen best seen on T2-weighted sequences were thought to represent neural elements encased by tumor (Figure 1D). This unusual extension of tumor was thought to extend along the lower cranial nerve complex suggestive of a

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malignant nerve sheath tumor, meningioma, ependymoma or intermediate grade glioma given the prolonged duration of symptoms. MRI of the cervical, lumbar and thoracic spine and

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cerebrospinal fluid cytology revealed no evidence of disseminated disease. In addition, a renal ultrasound was obtained which revealed no concomitant disease with normal sized kidneys for age and no metastatic lesions or hydronephrosis.

Operation A modified extreme lateral infrajugular transcondylar (ELITE) approach was used in this case. Whereas a standard ELITE approach involves partial resection of the medial and superior occipital condyle and jugular tubercle, the modified approach minimizes manipulation of the

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condyle and allows for an under-developed tubercle as is frequently encountered in children. Facial nerve, auditory brainstem evoked potentials, somatosensory evoked potentials, motor evoked potentials, and monitoring of cranial nerves X, XI, and XII were carried out throughout

accessory, vagus, and glossopharyngeal nerves.

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Follow-up Neuroimaging

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the surgery. Intradural tumor removal was then accomplished with preservation of the

Magnetic resonance images obtained post-operatively showed complete resection of the large

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exophytic brainstem component of the tumor with improved hydrocephalus. The tumor extending into the right jugular foramen remained unchanged (Figure 2).

Pathological Findings

Histological examination of the surgical specimen showed large pleomorphic cells with

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prominent nucleoli, eccentric nuclei with eosinophilic globular cytoplasm and numerous mitoses. Immunohistochemical evaluation revealed absence of INI-1 staining confirming the diagnosis of ATRT (Figure 3). Tumor was sent for sequencing that revealed SMARCB1 loss further

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confirming the diagnosis.

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Postoperative Course

Postoperatively patient showed gradual improvement in his cranial nerve palsies but had persistent lower cranial nerve neuropathies mainly with difficulty clearing his secretions. He was independently able to protect his airway after injection of voice gel and therefore, although discussed, did not require tracheostomy placement. However, there was still concern of aspiration with difficulty handling his secretions so a gastrostomy tube was placed for nutritional supplementation, which he required temporarily. His treatment included focal intensity modulated radiation therapy to the tumor bed (28 fractions of 180 cGy for a total of 5040 cGy)

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with adjuvant systemic and intrathecal chemotherapy without evidence of disease progression 2

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years post diagnosis.

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Discussion ATRTs are highly malignant intracranial neoplasms occurring in infancy and early childhood with a mean age of diagnosis at 29 months. (35) Children diagnosed with ATRTs often die within

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months to a year of diagnosis due to the high incidence of leptomeningeal dissemination at the time of diagnosis. (14, 26) A recent prospective study in patients with ATRTs using an intensive multi-modality treatment regimen has shown some improvement in prognosis but overall

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survival still remains low. (2, 6, 32) Resectability of the tumor and age at diagnosis have been implicated in predicting prognosis. (14, 19, 33) Although ATRTs are primarily malignant brain

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tumors of infancy and early childhood, there have been some reported cases of adult-onset ATRTs. Overall there have been very few cases of ATRT reported in teenagers, young adults and adults with only about 30 adult cases reported to date. (31) A Surveillance, Epidemiology, and End Results (SEER) Program data analysis looking at 144 patients over a period of 35 years (1973-2008) reported 82% of patients to be younger than 3 and only 2% of the patients

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older than 18 years, illustrating the rarity of ATRTs in the older pediatric population. (5) ATRTs do however need to remain in the differential diagnosis of malignant brain tumors in young adults as was shown by a case report of an ATRT in an 18 year old (28) as well as a series

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which included one teenage patient in a cohort of 20 patients with a confirmed diagnosis of ATRT. (6) The most common site for ATRT in adults is in the cerebrum whereas in children it is

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most common in the posterior fossa. While prognosis continues to be poor in young children, a small case series in adults showed improved survival in adults suggesting that depending on location ATRTs may be less aggressive in adults. (21) Advances in aggressive and early multimodal treatments may be contributing to improved outcomes. (14)

Jugular foramen tumors are extremely rare entities and tend to arise from the glomic tissue of the jugular vein. (13) The differential diagnosis of tumors with similar invasive jugular foramina characteristics includes meningioma, schwannoma, glomus jugulare, chondrosarcoma,

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myxoma, and PNET. A recent review of non-glomic tumors of the jugular foramen revealed that the most common tumor was a schwannoma followed by meningioma, which correlates with

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previous reviews of these tumors. (13)

ATRTs do not have specific neuroradiographic features, but in general are more often intraaxially positioned and of large size with some component of calcification, hemorrhage or

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necrosis on neuroimaging. (22, 23, 25, 36) When the radiologic features of ATRT in adult

patients were reviewed, the majority showed high density on CT, high intensity on DWI, and

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heterogeneous contrast enhancement with or without components of hemorrhage or calcification.(16) Unusual locations for the tumor have also been reported (15, 16) and therefore ATRT should be included in the differential diagnosis of any aggressive tumor regardless of the location or age of patient.

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The patient’s presentation and imaging features were unusual in that he had a long-standing history of progressive symptoms and presented at an atypical age with unusual tumor extension into the jugular foramen suggesting the origin of the tumor being in the jugular foramen. There

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have been several reported cases of patients with jugular foramen tumors who presented primarily with lower cranial nerve palsies, (7, 11, 34) as with our patient, due to the

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neurovascular structure that traverses this conduit. (20) Surgical management alone is often inadequate to cure even the less aggressive tumors that arise from this location due to the proximity to vital structures. However, to date, no cases of ATRTs extending from the jugular foramen have been reported. Although extremely rare, there have been isolated case reports of children presenting with jugular foramen tumors, which include schwannoma, PNET, meningioma, and subependymoma. (1, 8, 18, 29, 30)

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Conclusions This case highlights the atypical presentation, neuroimaging features, and challenges of treating such invasive nature of ATRTs and expands the differential diagnosis of tumors invading the

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jugular foramen.

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Figure Legends:

Figure 1 A-B. Contrast-enhanced coronal CT, soft tissue (a; W=97; L=71) and bone (b;

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W=2000; L=500) demonstrate a heterogeneously enhancing mass in the right posterior fossa, extending into the right jugular foramen (arrow, A). A necrotic focus is identified in the superior aspect of the mass on this image. There is expansion and remodeling of the jugular fossa

(arrow, B), compared to the contralateral normal side, suggesting gradual enlargement of the

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neoplasm. C. MRI reveals reduced diffusivity of the tumor on DWI sequences with extension into the jugular foramen (arrow, C). D. T2-weighted imaging reveals the exophytic component of

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the tumor with encasement of the cranial nerve complex as it enters the jugular foramen (arrow, D).

Figure 2. Post-operative axial (left) and coronal post-gadolinium sequences (right) reveals resection of the brainstem exophytic components of the tumor and residual neoplasm within the

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jugular foramen (arrows).

Figure 3. Hematoxylin and eosin staining (left) reveals a pleomorphic tumor including rhabdoid cells with eccentric nuclei and abundant eosinophilic cytoplasm, pale staining nuclei with large

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nucleoli, and mitotic activity (1000x). INI-1 immunohistochemistry reveals loss of INI

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immunoreactivity in tumor cells (right) consistent with a diagnosis of ATRT.

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Atypical Teratoid Rhabdoid Tumor in a Teenager with Unusual Infiltration Into the Jugular Foramen.

Atypical teratoid rhabdoid tumor is a rare malignant neoplasm that represents 1%-2% of all pediatric central nervous system tumors. Immunohistochemist...
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