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��XMultidisciplinary staged resection of endolymphatic sac tumor in a 14-year-old boy. 
Case report and review of the literature.

Ali Shirzadi, M.D.1

Debraj Mukherjee, M.D., M.P.H.1

Michael J. Alexander, M.D.1

Lee Tan, M.D.2

Serguei I. Bannykh, M.D., Ph.D.1

Rick A. Friedman, M.D.3

Keith L. Black, M.D.1

Moise Danielpour, M.D.1

1 Maxine Dunitz Neurosurgical Institute
Department of Neurosurgery
Cedars-Sinai Medical Center
8631 W. 3rd Street; Suite 800 East
Los Angeles, CA 90048

2 Department of Neurosurgery
Rush University Medical Center
1653 W. Congress Parkway
Chicago, Illinois 60612

3 House Ear Institute
2100 W. 3rd Street, Suite 111
Los Angeles, CA 90057

Running Title: Multidisciplinary resection of a pediatric endolymphatic sac tumor

Disclosure Statement: The authors have nothing to disclose.
Keywords: Endolymphatic sac tumor, temporal/petrous/mastoid bone tumor, von Hippel-Lindau.

Corresponding Author:
Debraj Mukherjee, M.D., M.P.H.
Maxine Dunitz Neurosurgical Institute
Department of Neurosurgery
Cedars-Sinai Medical Center
8631 W. 3rd Street; Suite 800 East; Los Angeles, CA 90048
Telephone: 310-729-1247 / Fax: 310-423-0810
E-mail: debraj.mukherjee@cshs.org
ABSTRACT

Endolymphatic sac tumors (ELSTs) are rare, low-grade, histologically benign tumors arising from the epithelial lining of the endolymphatic duct or sac. They are slow growing but locally invasive and can be associated with von Hippel-Lindau disease. While there are cases in the medical literatures documenting this type of tumor in adults, reports of ELSTs in the pediatric population are limited. 

The authors report the fifth widely reported case of a pediatric ELST, in a 14-year-old Jehovah�s Witness who presented with a progressive two-year history of  right-sided hearing loss, balance and gait difficulty, and bleeding behind the right tympanic membrane. CT and MR imaging revealed a large lesion eroding into the petrous and mastoid bones with extension abutting the brain stem and invading the right transverse sinus. Due to the size and hypervascularity of the tumor, as well as the patient�s refusal to receive blood products, pre-operative tumor embolization and staged surgical resection were used for excision of the tumor. Histopathological staining and electron microscopy confirmed the diagnosis of ELST.

Immediate post-operative imaging did not reveal any evidence of residual tumor. Post-operative examination revealed persistent right-sided hearing loss and facial nerve paralysis up to 21 months post-resection. MRI remained stable up to nearly one year post-resection, but routine imaging at 21 months follow-up did reveal recurrent tumor. The workup for von Hippel-Lindau disease has been negative. 

INTRODUCTION

Endolymphatic sac tumors (ELSTs) are rare, low-grade, locally invasive tumors of neuroectodermal origin arising from the pars rugosa of the endolymphatic sac or duct in the posterior part of the petrous temporal bone.19, 28 Often presenting with symptoms including tinnitus, vertigo, hearing loss, or various cranial nerve deficits, ELSTs can also be associated with von Hippel-Lindau disease.32 
Hassard first described a papillary adenomatous tumor that adheres to the endothelium of the endolymphatic sac in 1984.11 Heffner proposed the endolymphatic origin of this tumor type through a review of the histological and immunochemical features of 20 temporal bone tumors in 1989.12 Subsequently in 1993, Li coined the term �endolymphatic sac tumors�.18 
With an average age of presentation in the 5th decade of life, few pediatric cases of ELSTs have been reported in the literature.9-10, 17, 22, 27-28 This is the only reported case of pediatric ELST in a Jehovah�s Witness and details a multidisciplinary approach to resection of a pediatric ELST, including the use of pre-operative embolization as well as planned operative staging. 
CASE REPORT

History and Examination

A 14-year-old male Jehovah�s Witness presented with a 2-year history of progressive right-sided hearing loss and difficulty with gait and balance. On physical examination, he was morbidly obese with complete hearing loss in the right ear, ataxia, and old blood behind the right tympanic membrane. His facial nerve exam was normal.
Diagnostic Studies
Computed topography (CT) of the brain demonstrated an enhancing, partially calcified mass in the region of the right temporal bone. The lesion involved the petrous ridge and right sigmoid sinus with mass effect upon the right brachium pontus. Erosion of the posterior margin of the wall of the right internal carotid artery as well as the right jugular formen could also be appreciated (Figure 1). Magnetic resonance imaging (MRI) of the brain revealed a 6.3 x 4.7 x 3.6 centimeter expansile mass centered in the right posterior petrous temporal bone with extension to the right cerebellopontine angle with multiple fluid-fluid levels; it had, central areas of T2 hypointensity and enhancement, and scattered areas of T2 hyperintensity consistent with chronic hemorrhage (Figure 2).  CT scan of the chest, abdomen, and pelvis did not reveal other lesions consistent with von Hippel-Lindau disease.

Operation

Due to the hypervascularity of ELSTs, coupled with diagnostic imaging concerning for vascular compromise and the patient�s wish not to receive blood products, the patient was first taken to the interventional suite for pre-operative diagnostic angiogram and embolization of the tumor. Selective right internal carotid cerebral angiogram revealed mild tumor blush from the cavernous branches of the internal carotid artery. Selective right external carotid artery angiogram revealed a large tumor blush in the right petrous temporal bone region and posterior fossa (Figure 3A). Additionally, there was evidence of arteriovenous shunting in the tumor with early venous filling to the paracervical venous plexus. Multiple feeders to the tumor were also revealed. The four most prominent feeders to the tumor, including one feeder from the occipital artery, two feeders from the middle meningeal artery, and two feeders from the posterior auricular artery, were successfully embolized using polyvinyl alcohol particles measuring between 45 to 150 microns in size. Post-embolization angiography demonstrated a modest reduction in the amount of tumor blush (Figure 3B).
The patient was taken to the operating room one day1 following tumor embolization, for staged surgical excision of the tumor. A combined petrosal and middle temporal fossa skull-base approach was used for tumor resection. The tumor infiltrated a large portion of the sigmoid sinus and also encased the facial nerve from the horizontal segment at the geniculate to the stylomastoid foramen. Because of the local invasiveness of the tumor, coupled with the high rate of recurrence from partial resection of ELSTs, we proceeded with complete removal of the tumor from the middle ear to the portion involving the facial nerve.  Once the patient�s blood loss had reached 800 milliliters, we elected to stop the operation and return for completion resection at a later date so as to eliminate the need for immediate blood transfusion. The patient did receive CellSaver (Haemonetics, Braintree, MA), which the patient and family agreed to prior to surgery.
Five weeks later, the patient was taken back to the operating room for the second stage of tumor resection. The previous incision was reopened and extended both to the pre-auricular and retrosigmoid skull base. A right-sided infratemporal/postauricular/transjugular approach was use to access the middle cranial fossa, including the auditory meatus, petrous apex, tentorium, and infratemporal fossa. The tumor was infiltrating into the dura at multiple sites. The affected dura was carefully resected, repaired with a dural patch graft, and dead space was filled with abdominal fat graft. Blood loss during the second operation was 300 milliliters.

Pathological Findings

Pathological sections of a soft, pink-yellow colored, formalin-fixed tumor specimen revealed papillary arrangements of bland cuboidal to columnar cells forming monolayers and containing round to oval nuclei with no discernible mitotic activity. There were also areas of hemosiderin-laden macrophages, infiltrates into bony trabeculae, and some papillae demonstrating cystic degenerative changes in the stroma (Figure 4A). Methylene blue-stained sections of glutaraldehyde/osmium-fixed and Epon plastic-embedded material revealed papillary growth of tumor cells with minimally osmophilic subnuclear vacuoles associated with glycogen-like staining material, no mitotic activity, and no necrosis (Figure 4B). All histopathological findings were consistent with endolymphatic sac papillary tumor.
Ultra-thin sections examined under electron microscopy revealed polarized epithelial cells containing predominantly electron-lucent granules consist with mucin. Electron microscopy further revealed nuclei with an open chromatin pattern, inconspicuous nucleoli, and no mitoses. The cytoplasm was moderate in amount and contained elements of rough endoplasmic reticulum, Golgi complexes, mucin vacuoles, and abundant glycogen particles. The lateral surfaces of the cells were smooth and connected by numerous cellular junctions, including tight junctions, true desmosomes, and adhesive junctions, with predominantly subapical keratin-like filaments attached. The basal surface of cells contained numerous interdigitations, while the apical surface of cells were studded with microvilli and only rare cilia (Figure 4C).

Post-operative Course

At four month and twenty-one month following-up, the patient�s physical examination was unchanged relative to his immediate post-operative examination, including a persistent House-Brackmann grade 4 right facial nerve paralysis and complete hearing loss of the right ear. Four month, eight month, and 12 month post-operative imaging did not show any evidence of tumor recurrence (Figure 5).  The patient and family were not compliant with post-one year follow-up recommendations and subsequent routine imaging twenty-one months post-intervention did reveal recurrence (Figure 6). Options for surgical resection versus Gamma Knife therapy were discussed with the patient and family. Given this recurrence, the family is currently considering re-operation versus Gamma Knife therapy. The possible use of radiosurgery for recurrence was, in part, based upon recent reports in the literature demonstrating the efficacy of delivering up to 15 Grays of radiation to recurrent ELST tumors with no further recurrence through up to 3 years of follow-up.4, 
DISCUSSION
Endolymphatic sac tumors (ELSTs) are rare, low-grade, hypervascular, invasive tumors arising from the epithelium of the endolymphatic sac or duct and found in approximately 11% of patients with von Hippel Lindau (VHL) disease. They most commonly present with an insidious onset of hearing loss, facial nerve palsy, or other cranial nerve deficits in patients most commonly in their fifth decade of life or older. Tumors less than 3cm in diameter are usually fed by ECA branches, whereas tumors greater than 3cm usually have additional feeders from the ICA and posterior circulation.26 The dural branches of the ascending pharyngeal and stylomastoid artery usually supply these tumors. Larger tumors can have blood supply from the ICA or posterior circulation.23 Treatment of choice for ELST is complete excision with wide-margins given the long disease-free survival of patients in previous series following gross total resection, as well as the relative radio-resistance of these tumors. 
ELSTs have been shown to be associated with VHL disease in some cases, and extensive research has been devoted in studying the VHL gene in relation to ELSTs.7-8, 13-15, 25, 30-31 VHL-associated ELSTs were shown to have a earlier age of onset compared to the sporadic form of the disease in a study with 149 patients by Bambakidis et al (31.3 years old for VHL patients and 52.5 year old for non-VHL patients).5 Bilateral ELSTs are also more common in patient with VHL disease.5, 20 Patients with VHL often have concomitant conditions, such as retinal hemangiomas, intracranial hemangiomas, renal cell carcinomas, pancreatic cysts and pheochromocytomas.10 Metastasis of ELSTs is exceedingly rare, with only 2 cases of drop metastases to spine having ever been reported.6, 29 
On CT imaging, ELSTs usually present as a retrolabtrinthine mass with an epicenter in the retrolabyrithine/presigmoid area, growth in all directions, and destruction of adjacent structures. On MRI, a hyperintense foci  on T1 and T2 sequences (�salt on pepper� appearance) with heterogeneous enhancement both on T1 and T2 sequences is appreciated.2, 26 Radiographically, ELSTs can be misdiagnosed as paraganglioma, hemangioperictoma, chondrosarcoma, or plasmacytoma due to similarities on CT and MRI imaging.29
Histologically, ELSTs may appearance similar to metastatic thyroid cancer, renal cell cancer, or paraganglioma. ELSTs, however, classically have the appearance of colloid filled cysts lined by a single layer of cuboidal to columnar cells with basally displaced nuclei and glycogen vacuolations.16, 24 ELSTs have positive immunochemical reactivity for CAM 5.2, epithelial-marker antigen (EMA), and glial fibrillary acidic protein (GFAP).19 ELSTs also have immunoreactivity for cytokeratin and S100.16
Treatment of choice for ELSTs is complete excision with wide-margins. A retrolabyrithine approach may be used if hearing is preserved. If the tumor has invaded the labyrinth, a translabyrithe or transcochlear approach can be used. Heffner et al. reported a 90% cure rate with total resection, whereas 71% of patients with partial tumor resection followed by radiotherapy developed recurrence/regrowth of ELSTs over an average follow-up period of 5.7 years.12 Twelve of fourteen (85.7%) patients with complete resection remained disease-free over an average follow-up period of 59.4 months in another study by Hansen et al., further supporting complete resection as the treatment of choice.10 Additionally, two studies have shown ELSTs to be relatively radio-resistent.12, 21 However, a case report by Balasubramaniam et al. demonstrated the efficacy of delivering 15 Grays of radiation to a recurrent ELST tumor, though the follow-up period in this report was only 3 years.4 Long-term survival data in patients with ELST have not been widely reported through the literature, though patients with drop metastases to the spine appear to have poor long-term survival.1, 6, 29
The patient in this case was only 14 years old, much younger the most patients presenting during their middle-age years. Additionally, this patient represents the only Jehovah�s Witness pediatric case of ELST in the literature. While most patients present with an insidious onset of symptoms over many years, this patient developed symptoms over a relatively short course of only two years, much more acutely than the 4 year course of symptoms demonstrated in the case report of an 11-year old with ELST by Ferreira et al.9 Similar to the case reports by Ferreira et al. and Kupferman et al., our patient presented with hearing loss, though our patient did not present with facial nerve paralysis, as did the Ferreira and Kupferman patients.9, 17 Aside from this child, Bae et al. and Megerian and Semaan have reported the only other patients described in the literature thus far to have presented with vertigo.3, 22 
Although the use of pre-operative embolization and staged procedures for removal of ELSTs in children has been reported before by both Ferreira et al. and Bae et al., this report represents the first to specify technical aspects of the actual embolization technique utilized.3, 9 While the reports by Ferreira and Bae both described embolization of occipital feeders into ELSTs, this report additionally notes the first embolization of arterial feeders from the middle meningeal artery and posterior auricular artery.3, 9  Additionally, this case represents the first description of an initial combined petrosal/middle temporal fossa skull-base approach followed by an infratemporal/postauricular/transjugular approach to resect an ELST. All previous reports within the pediatric literature have exclusively utilized a  translabyrinthine approach (Table 1).3, 9, 17, 22 
Care of our patient was also complicated by the patient�s religious beliefs, precluding use of blood transfusions. Though previous reports have not specified their operative blood loss, the standardized use of pre-operative embolization in patients, particularly children, seeking to minimize operative blood loss during resection of these hypervascular lesions may serve as a helpful adjuvant tool to the operating room in the future.
The presentation of this case is limited in several respects. First, the follow-up time period for this patient following his second, completion resection is only 21 months, as opposed to the 4.5 year follow-up of the Ferreira et al. case.9 However, our follow-up is significantly greater than the 6 month follow-up of the Kupferman et al. case.17 Nevertheless, our relatively short follow-up period does limit our ability to comment on pertinent long-term follow-up issues, including the need for potential future radiosurgery or reoperation. Additionally, our screening for von Hippel Lindau disease included primarily an imaging survey for additional lesions via CT scanning. A more robust work-up may have included genetic testing. 
CONCLUSION 

ELSTs are rare tumors, with pediatric cases being exceedingly rare. The hypervascularity of these tumors pose potential challenges in surgical resection due to higher risks of bleeding. However, with pre-operative embolization of feeder arteries, utilization of Cell Saver intraoperatively, and with carefully planned operative staging, complete resection of these tumors is possible. Even in patients in whom a gross total resection is achieved, routine post-operative imaging should be pursued to evaluate for possible recurrence.
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FIGURE LEGEND

Figure 1. Pre-operative CT of the brain demonstrated an enhancing partially calcified mass of the right temporal bone with mass effect upon the right brachium pontus.

Figure 2. Pre-operative MRI demonstrating an expansile mass in the right posterior petrous temporal bone with extension to the right cerebellopontine angle, multiple fluid-fluid levels, and signs of chronic hemorrhage.

Figure 3. Selective right external carotid artery angiogram demonstrating a large blush in the right petrous temporal bone region and posterior fossa consistent with feeders to the ELST from the occipital artery, middle meningeal artery,and posterior auricular artery pre-embolization (A) with only minimal blush post-embolization (B).

Figure 4. (A) Hematoxylin and eosin staining, (B) methylene blue-staining, and (C) electron microscopy imaging confirming the diagnosis of ELST.

Figure 5. Post-op MRI one-year following completion resection demonstrating no evidence of tumor recurrence.

Figure 6. Post-op MRI twenty-one months following completion resection demonstrating evidence of tumor recurrence.

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