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Cranial nerve root entry zone primary cerebellopontine angle gliomas:a rare and poorly recognized subset of extraparenchymal tumors
Kenan 1. Arnautovic l , Muhammad M. Husain2.3 and Mark E. Linskey II Departments ot' Neurological Surgery and 2Pathology, University ofArkansasfor Medical Sciences;'Laboratory Service, John McCleLLan VA Hospital, Little Rock, AR, USA
Key words: brain tumor, cerebellopontine angle, gl ioma, pilocytic astrocytoma, cranial nerve glial segment,cranial nerve root entry zone, trigeminal nerve
With the exception of patients with neurofibromatosis type II, pediatric extraparenchymal cerebellopontine angle(CPA) tumors of any sort are extremely rare. Most gliomas encountered in the CPA in either children or adults involvethe CPA as exophytic extensions of primary brain stem and/or cerebellar tumors. We encountered an unusual case of agiant CPA pilocytic astrocytoma arising from the proximal trigeminal nerve, completely separate from the brain stem.A nine-year-old girl with no evidence for any neurocutaneous syndrome, presented with headaches, mild obstructivehydrocephalus, trigeminal hypesthesia and a subtle peripheral facial paresis. Pre-operative neuroimaging suggesteda petroclival meningioma. The tumor was completely resected via a right pre-sigmoid, retro-Iabyrinthine, sub-teillporal, transtentorial ('petrosal') approach, using intraoperative neurophysiological monitoring, with minimalmorbidity. This appears to be the first reported case of a pediatric primary CPA glioma and the seventh reportedcase of primary CPA glioma, overall. It represents the second reported case of a primary CPA pilocytic astrocytoma.Given the findings in this case and the six other cases of primary CPA gliomas reported in the literature, as wellas the results of histological studies of normal cranial nerves, we hypothesize that the point of origin of these rareand unusual tumors is the root entry zone of the involved cranial nerves. The differential diagnosis of primary CPAtumors should be expanded to include cranial nerve root entry zone primary CPA gliomas.
Extra-axial cerebellopontine angle (CPA) tumorsaccount for approximately 10% of all intracra-nial tumors in adults, but only 0.2-3% of poste-rior fossa tumors in children. A large portion ofthese are found in children with neurofibromatosistype II (NF2) with bilateral vestibular schwanno-mas. In children without NF2, CPA tumors are evenmore rare. The differential diagnosis of CPA tumorsincludes cranial nerve schwannomas (vestibular mostcommon), meningiomas, neurofibromas, metastatictumors, epidermoid, dermoid and arachnoid cysts,ependymomas, choroid plexus papillomas, lipomas,medulloblastomas, ependymoblastomas, glomus jugu-lare tumors, cholesteatomas, and exophytic brain stemgliomas [4,5,7,9-17,19,23,24,26,31,34,36].
Exophytic brain stem gliomas are rare. Most casesreported in the literature have been either fibrillary
or gemistocytic astrocytomas [5,14,16,19,31]. Whilepilocytic astrocytomas are common in children, espe-cially in the posterior fossa, they are almost alwaysintraparenchymal in origin and are rarely exophytic innature. The literature suggests that all but six gliomas,of any sort, encountered in the CPA have been exo-phytic extensions of a brain stem glioma. Beutler andcolleagues repolted a single case of a pilocytic astrocy-toma arising from the eighth cranial nerve, completelyseparate from the brain stem. Five additional extra-axial non-pilocytic CPA gliomas have been reportedarising from the eighth nerve. All six occurred in adults[4,8,17,27,31].
We recently encountered a giant pilocytic astrocy-toma in the CPA of a child arising from the proximaltrigeminal nerve, completely separate from the brainstem. Pre-operatively, neuroimaging had strongly sug-gested a petro-clival meningioma. Since cranial nerveeight and five have the first and second longest root
entry zones, respectively, of any cranial nerve (opticand olfactory nerves excluded), it is likely that both ourcase, and six previously reported cases, arose from theroot entry zone of the cranial nerve.
Presenting symptoms and neurological findings
A nine-year-old, right-handed, African American girlpresented to our Emergency Room with a two monthhistory of intermittent headaches, significantly increas-ing in intensity over the past two weeks. They wereaccompanied by nausea and vomiting 2-3 times perday for the last four days. The patient's mother alsoreported one 'blackout' episode that has occurred onthe morni ng of presentation. Her past medical, surgicaland family histories were all noncontributory.
On general physical examination she had no occulo-cutaneous stigmata of any neurocutaneous syndrome.There was no papilledema. Neurological examina-tion revealed right-gaze horizontal nystagmus, but fullextra-ocular movements without diplopia. The rightcorneal reflex was significantly decreased. Light touch
sensation in her right V 1-3 distribution was decreased;pinprick sensation in the same area was preserved. Shehad House-Brackmann grade 2 facial function on theright r14]. Hearing tested by audiogram was normaland symmetric. Gag, voice, and swallowing functionwere normal. Tests for dysmetria and dysdiadokine-sis revealed relative impairment on the right. Gait wasmoderately ataxic. The rest of her neurological exam-ination was normal.
Computerized tomography (CT) scan revealed adiffusely-enhancing, hypodense, right extra-axial,petro-ciivaJ CPA mass with an apparent broad lin-ear base along the posterior surface of the petrousbone (Figure I). Magnetic resonance imaging (MROrevealed a diffusely enhancing giant extra-axial CPAtumor (3.5 cm x 4 cm x 4.5 cm) with significant brainstem, fourth ventricular, and cerebeJlar compression(Figure 2). The tumor was hypointense on shortTR, and strongly hyperintense on long TR sequences(Figures J and 2). Magnetic resonance angiography(MRA) demonstrated relative right-sided dominance of
Figure I. A: Unenhanced axial cerebral CT scan of demonstrating a giant right hypoclense petro-clival CPA tumor C). B: Postcontrastaxial cerebral CT scan demonstrating homogenous enhancement of the tumor ("').
Figure 2e & f A. Noncontrast axial short TR MR image reveaJing a hypoll1tense giant nght petro-cliva! CPA tumor (") (TR 400/TE16INEX I); B: Same image after contrast enhancement reveallnga brightly and homogeneously-enhancing tumor e) (TR4001TE 16/NEXI); C: A long TR un-enhanced MR image revealing a hypenntense CPA tumor C) (TR 2500ITE 30/NEX 0.75); 0: Postoperative contrast-enhanced axial MR image demonstrating gross total tumor removal. Note the fat graft (") placed ll1 position of driJJed petrous bone (TR400ITE 16/NEX I), E. Coronal contrast-enhanced short TR MR Image revealing a bnghtly homogeneously-enhancll1g CPA tumor ("').Note the brall1 stem compression (TR 400ITE 16INEX J) p. Post-contrast postoperative coronal short TR MR Image confirming grosstotal tumor removal and relief of brall1 stem compression. Note the fat graft (*) placed 111 position of drilled petrous bone (TR 400/TE16/NEX I)
transverse/sigmoid sinus. The tumor itself had a faintreticular tumor blush on MRA.
The lesion was approached via a right pre-sigmoid,retro-Iabyrinthine, sub-temporal, trans-tentorial('petrosal') approach [2,3] with somatosensory evokedpotential (SEP), brain stem auditory evoked response(BAER), and facial nerve electromyography (EMG)intraoperative monitoring. Upon dural opening andtentorial sectioning, we encountered a gray-green,apparently encapsulated, relatively poorly vascular-ized tumor, grossly felt to be a schwannoma. Preservedarachnoid cistern planes allowed us to successfullyseparate and elevate the tumor from the cranial nerveIX and X complex, the cranial nerve VII and VII
complex, and the anterior inferior cerebellar arteryinferiorly. Frozen section biopsy surprisingly returneda diagnosis of 'low grade astrocytoma'.
The tumor center was debulked using a cavitronultrasonic aspirator until the tumor capsule becamemobile. A clear arachnoid cleavage plane was presentalong the interface between tumor and the cerebel-lum, middle cerebellar peduncle, and the pons. Thetumor was found to arise from the proximal trigeminalnerve distal from its brain stem origin. The nerve itselfwas atrophic and thinned to a widened and diaphanoussuperior 'cap' over the tumor. A gross total tumor resec-tion was achieved with all surrounding anatomic struc-tures preserved. An abdominal fat graft was harvestedand placed in the position of the drilled bone (tempo-ral mastoid). Neurophysiologic monitoring during thesurgery remained un-perturbed.
Her postoperative course was uneventful. Herheadache, nystagmus, mild facial nerve dysfunction,and cerebellar findings resolved postoperatively. Hertrigeminal function remained intact for motor function,but was worse for light touch and pinprick sensationpostoperatively. Her corneal reflex was absent on theright. Eye protection lubricants were prescribed. Theremainder of her neurological examination remainednormal. She was monitored for two days in the intensivecare unit, and discharged home after a total of one weekof hospitalization. Postoperative MRI confirmed grosstotal tumor resection (Figure 2D and F). No recurrencewas noted on follow-up MRls during the past year.
Histolog iCC/I findings
Gross pathological examination revealed multiplesmall pieces of pale, gray-pink, gelatinous tumor.Microscopic examination revealed a low-grade glial
neoplasm. The tumor demonstrated a biphasic patterncomposed of bundles of elongated glial cells mixedwi th areas of microcavi tary change. The cells were thin,somewhat elongated, and had small, oval shaped nucleiin the background of fibrillary glia with many Rosen-thal fibers. There was no vascular proliferation, mitosisor necrosis. These histopathological features were typ-ical for pilocytic astrocytoma (Figure 3).
CPA tumors and primary versus secondary CPAgliomas
CPA tumors represent about 10% of all intracra-nial tumors in adults. Vestibular schwannomas arethe most common (80%) followed by meningiomas(10%). The remaining 10% includes a variety of otherlesions including: other cranial nerve schwannomas,
Figure J. Representative histology; hematoxylin-eosin stain, original magnification x33; A: Upper half: Solid area of the tumor. Notetbe occasional Rosenthal fibers which can be seen even at this low magnification; Lower half: Cystic area of a tumor; B: Solid tumor area.Note abundant Rosenthal fibers (original magnification x J 32).
Figure 4. Artist's rendition of the cranial nerve segments demon-strating r.he locar.jon of r.he glial segment, the location and shapein longitudinal cross secr.ion of the r.ransir.ion zone ancl r.he loca-tion of the peripheral (Schwann) segment. The root entry zoneincludes both the glial segment and the transition zone (fashioned
after references 6,32,33,35, and 36).
metastatil: tumors, epidermoid, dermoid and arachnoidcysts, ependymomas, neurofibromas, cholesteatomas,glomus jugulare tumors, choroid plexus papil-lomas, Iipomas, medulloblastomas, ependymoblas-tomas, and exophytic brain stem gliomas [4,5,7,9-17,19,23,26,31,34,36].
CPA gliomas are very rare and usually only secon-darily involve the CPA. They are most often exophyticextensions of primary brain stem fibrillary and gemis-tocytic astrocytomas [5,14,16,19]. We have been ableto find only six cases of truly primary CPA gliomaspublished in the literature [4,8,17,27,31]. In each case,the glioma arose from the eighth cranial nerve com-pletely separate from the brain stem. All six caseswere reported in adult patients, and only one of thesix gliomas was a pilocytic astrocytoma . The otherfive cases were either described non-specifically as'gl iomas' or were fibrillary astrocytomas [8,17,27 ,31].
GlialLS,gm,otRoot Entry Zone
Pilocytic astrocytomas remain the most common solidtumors, brain tumors and posterior fossa tumors inchildren. Sex distribution is roughly equal. In the pos-terior fossa, they occur either in the cerebellum orin the brain stem. Regardless of their point of ori-gin, the majority of these lesions remain intrinsicparenchymal tumors. On the rare occasion where theydo extend exophytically from their point of originthey usually fungate dorsally, spreading the tonsils ofthe cerebellum, and only rarely extend into the CPA[1,11,15,18,20,21,28,29,35,36].
An extra-axial pediatric primary CPA pilocyticastrocytoma has not been previously reported. [nfact, excluding bilateral vestibular schwannomas inpatients with NF2 , pediatric CPA tumors areexceedingly rare, and only include several publishedcases of schwannomas, chordomas, ependymomas andsecondary fibrillary and gemistocytic astrocytomas[7,19,23,31]. We have been able to identify only oneother previously reported case of primary CPA pi 10-cytic astrocytoma and this tumor arose in an adultpatient. It was small in size, and took origin from theVIJl cranial nerve complex .
The cranial nerve glial segment (root entry zone)as a sourcefor primary CPA gliomas
Cranial nerves contai n three histologically distinct seg-ments: the glial segment, a transition zone and a
peripheral segment (Figure 4) [6,32,33]. The cranialnerve root entry zone refers to the maximum possiblelength of proximal cranial nerve where glial axon insu-lation may still be present, and includes both the glialsegment and the transition zone. The glial segment isadjacent to the brain stem and is histologically identi-cal in structure to a central nervous system white mat-ter tract, where nerve axons are supported by neuroglia(both astrocytes and oligodendrocytes). The peripheralsegment is histologically similar to a peripheral nerve,where the nerve fibers are insulated and supportedexclusively by Schwann cells. Between these two seg-ments lies an intermediate or transition zone of varyinglength. This transition zone is 'helmet-shaped' in lon-gitudinal cross section, ex tend ing for a greater distancewithin the center of the nerve compared with the cir-cumferential periphery . Even beyond the root entryzone, occasional isolated 'glial islands' have been iden-tified on histological sections of the peripheral segment[6,32,33,37,38]. Studies by Bridger and Farkashidi ,Lang , Skinner , Tarlov  and Ylikoski et at.[37,28] detailed the histology and systematically mea-sured the extent of glial outgrowth along the variouscranial nerves (Table I). Sensory cranial nerves havelonger root entry zones, than motor nerves. Excl ud-ing the optic [32,33] and olfactory  nerves, whichare direct extensions of the central nervous systemand have no peripheral segments, the longest glial seg-ment is found in the eighth cranial nerve, followed bythe sensory part of the fifth cranial nerve, and thenthe facial and glossopharyngeal nerves. The remainingcranial nerves have short « 1.9 mm) glial segments.
Table I. The mean (range) lengths of cranial nerve root entry lone segments reportedby different investigators in millimeters
Cranial nerve Cranial nerve root entry lOne length (mm)
Bridger and Lang  Skinner  Tarlov Farkashidi [61
I Total 0.5I! Total TotalIII 1.2 1.2IV 1.9 1.9V MotorV Sensory 3.6 (2-6) 3.0 2.2VI 0.5 0.5VlI 2.05 (0.5-4) 2.5 0.8Vlll 10.75'" 10 (6-15) 8.2 - cochlem' 8.0 - cochlear
9.0 - vestibular 8.3 - vestibularIX U 1.1X 1.0 1.3XI
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Address for oJjj;rints: Mark E. Linskey, DepaJ1ment of Neuro-logical Surgery. University of Arkansas for Medical Sciences4301 West Markham, Slot 507, Little Rock. Arkansas 72205:USA, Tel.: 501-686-5270; Fax: 501-686-7928; E-mail: [email protected]