DOI: 10.3171/2010.9.

SPINE09963

Multifocal intradural extramedullary ependymoma

Case report

Eduardo Augusto Iunes, M.D.,1 João Norberto Stávale, M.D., Ph.D., 2

Rita de Cássia Caldas Pessoa, M.D., 3 Ricardo Ansai, M.D.,1 Franz Jooji Onishi, M.D.,1
Manoel Antonio de Paiva Neto, M.D., Ph.D.,1 Antônio de Pádua Bonatelli, M.D., Ph.D.,1
Sérgio Cavalheiro, M.D., Ph.D.,1 and Suzana M. Fleury Malheiros, M.D., Ph.D.1
Departments of 1Neurology and Neurosurgery, 2Pathology, and 3Radiology, Universidade Federal de São
Paulo, Brazil

In this paper, the authors present the case of a patient with multifocal intradural extramedullary ependymoma,
and they review 18 previously reported cases.
A 32-year-old man presented to the authors’ institution with a 1-month history of partial medullary syndrome.
Magnetic resonance imaging of the neuraxis revealed multifocal intradural extramedullary lesions at the bulbomed­
ullary junction and C2–3, T5–11, L-2, L-4, L-5, and sacrum. Histological examination revealed a WHO Grade II
ependymoma.
The literature survey yielded 18 cases of ependymoma at the same location; none of them were multifocal at
presentation. The authors analyzed the epidemiological, clinical, and surgical features of all 19 cases reported to date,
including the present case.
Patients’ ages ranged from 24 to 69 years; 15 patients were women and 4 were men. The time elapsed from
symptom onset to diagnosis ranged from 1 month to 8 years. Pain (in 13 patients) and medullary syndrome (in 12)
were reported as the initial symptoms (information was not provided for 1 patient). Tumors were predominantly
located in the thoracic spine (11), but they also occurred in the cervicothoracic (3), cervical (2), and lumbar (2)
spine. The remaining tumor was multifocal. Solitary extramedullary tumors were found intraoperatively in 13 pa­
tients; 3 were described as exophytic and 3 as extramedullary with some degree of medullary invasion. Histological
examination revealed 9 WHO Grade II tumors, 4 Grade III tumors, and 1 myxopapillary tumor. Data obtained for
the remaining cases proved inconclusive. The clinical condition improved in 11 patients, remained stable in 2, and
worsened (recurrence or progression) in 6. Of the 4 patients with Grade II tumors who presented with recurrence or
neuraxis spreading, 3 had meningeal infiltration or adhesion to the pia mater, which does not rule out the possibility
of neoplastic remnants in that area.
Intradural extramedullary ependymomas are rare, they predominate in women in the 5th decade of life, and pain
is the most frequent initial symptom. The extent of resection and the presence of meningeal infiltration seem to be key
determinants of prognosis. The present case is the first intradural extramedullary ependymoma (with the exception of
those occurring at the conus medullaris and terminal filum) with multiple lesions at presentation.
(DOI: 10.3171/2010.9.SPINE09963)

Key Words      •      ependymoma      •      extramedullary ependymoma      •     

intradural ependymoma       •      multifocal ependymoma

S
pinal cord tumors can be classified as extradural
(55%) or intradural (45%), the latter being either in­
tramedullary (5%) or extramedullary (40%).22 Neu­­­­­ro­
fibromas, neuromas, and meningiomas account for roughly
60% of intradural extramedullary tumors and affect mainly
adults, whereas intramedullary tumors are more common
in children. Ependymomas and astrocytomas are the main
histological diagnoses in the children.22
Ependymomas are the most common intramedul­
lary tumors and occur predominantly in adults. The re­
ported cranial/spinal tumor ratio for ependymomas is
4:1, ranging from 3:1 to 20:1, depending on histological
subtype.18,19,22 Intradural extramedullary ependymomas
are extremely rare except for those located at the termi­
nal filum or conus medullaris.20,22 An extensive literature
survey yielded 18 such cases.3,5–7,9–14,17,21,23,24,27,29,31 The
present study reports the 19th case and reviews all cases
described to date.

J Neurosurg: Spine / December 10, 2010 1

 E. A. Iunes et al.

Fig. 1.  Sagittal T2-weighted (A and C) and fat-suppressed, postcontrast T1-weighted (B and D) MR images of the cervicotho-
racic region demonstrating multiple intradural extramedullary lesions in the bulbomedullary junction, C2–3, and T6–11 with high
signal intensity on the T2-weighted images, cystic areas, and moderate and heterogeneous enhancement. Note the irregular and
thickened enhancement outlining the posterior surface of spinal cord.

Case Report

History and Examination. This 32-year-old man pre­

sented with progressive paresthesia in the lower limbs,
gait disturbance, and urinary retention during the preced­
ing month. Neurological examination showed hypesthe­
sia at the T-9 level, lower-limb hyperreflexia, Romberg
sign, and calcaneal gait. Muscle strength was preserved.
Initial spinal MR imaging revealed multiple intradural
extramedullary lesions in the bulbomedullary junction
and C2–3, T5–11, L-2, L-4, L-5, and sacrum that were
predominantly isointense on T1-weighted images and
hyperintense on T2-weighted and FLAIR images, with
moderate contrast enhancement (Figs. 1 and 2). Cranial
MR imaging showed an interpeduncular nodular lesion
with mild contrast enhancement (Fig. 3).
Operation. A T7–9 laminectomy was performed at the
site of the major compression of the spinal cord according
to the MR imaging findings. A brownish intradural extra­
medullary tumor compressing the spinal cord posteriorly
was immediately apparent after opening the dura. Under
microscopic assistance, no attachment of the tumor to the
dura or spinal cord was observed, but arachnoid infiltra­
tion was noted. The tumor was soft. After internal debulk­
ing of the lesion, a sharp dissection at the tumor–spinal
cord interface was performed, and the tumor was resected.
Because of the multifocal characteristic of the lesion and Fig. 2.  Sagittal fat-suppressed postcontrast T2-weighted (left) and
T1-weighted (right) MR images of the lumbar spine demonstrating in-
arachnoidal infiltration, the aim of the surgery was spinal tradural and extramedullary entities appearing as cervicothoracic le-
cord decompression instead of total resection. The histo­ sions at the level of L-4 and L-5. Superficial enhancement is observed
logical examination revealed a WHO Grade II ependy­ in the conus medullaris.

2 J Neurosurg: Spine / December 10, 2010

Multifocal intradural extramedullary ependymoma
Fig. 3.  Postcontrast FLAIR (left) and T1-weighted (right) MR imag-
es of the brain showing an interpeduncular nodular lesion hyperintense
on the FLAIR image and with mild contrast enhancement.
moma with hypercellular nodules showing a Ki 67 index
of 10% (Fig. 4).
Postoperative Course. Postoperatively, the patient de­
veloped a transient motor deficit (strength 4/5 in the ilio­
psoas, quadriceps, tibialis anterior, extensor hallucis lon­
gus, and gastrocnemius muscles). He was able to stand on
his own and walk with assistance. The patient received ad­
juvant chemotherapy consisting of 4 cycles of carboplatin
(175 mg/m2/week for 4 weeks), followed by a 2-week break,
without objective response.
Ten months after surgery, the patient presented with
progressive paraparesis. He underwent a partial resection
of the intradural extramedullary lesion between T-9 and
T-10, which adhered to nerve roots without medullary in­
vasion. Histological examination again revealed a WHO
Grade II ependymoma. Regarding the intracranial lesion,
it was never biopsied, but it was assumed to have the same
histology because of the similarity of the MR imaging
characteristics. The tumor remained stable during follow-
up. The patient underwent radiotherapy at 39.5 Gy (whole
brain) and 36 Gy (neuraxis), but no objective response
ensued. He refused further chemotherapy and 8 months
later developed a complete spinal cord syndrome and
septic shock due to a urinary tract infection. The overall
survival was 105 weeks.
Discussion
We found 17 publications reporting 18 patients with
intradural extramedullary ependymoma (2 of them were
reported in a single publication by Hentschel et al.13). Ta­
ble 1 shows the demographic, clinical, and follow-up data
of all patients, including the patient in the present report.
Of the 19 patients, 15 were women and 4 were men.
A higher incidence among women has been observed in
earlier studies.9,12 In a review paper of intradural extra­
medullary ependymomas, Duffau et al.9 postulated that
a hormonal factor was involved. The higher prevalence
among females does not match epidemiological data on
spinal tumors, which affect males and females at simi­
lar rates, except for meningiomas, which are more com­
monly found among females, and intramedullary epen­
dymomas, which are more prevalent among males.18,19,22
J Neurosurg: Spine / December 10, 2010
Fig. 4.  Photomicrographs showing a moderately cellular ependymo-
ma with a monomorphic nuclear morphology and a perivascular pseu-
dorosette (A), perivascular pseudorosette (B), increased cellularity and
pleomorphic area with 1 mitosis (C), and ependymal rosette (D). H & E,
original magnification × 100 (A and B); × 400 (C and D).
Patients’ ages ranged from 24 to 69 years, a range similar
to that described for intramedullary cases, with predomi­
nance in the 5th decade of life.20,22
The initial symptoms were pain in 13 patients and
medullary syndrome (with motor and/or sensory and/or
sphincter control deficit) in 12 (data were not available for
1 patient). Dorsalgia and radicular pain are the most fre­
quently reported clinical symptoms, regardless of com­
partment (intra- or extradural) or histological subtype.22
Intradural extramedullary ependymomas tend to follow
the same pattern, with pain being reported as the earliest
symptom in the majority of cases described (13 [72.2%]
of 18 cases).
The time elapsed from symptom onset to diagnosis
ranged from 1 month to 8 years. The time interval from
the first clinical manifestation to diagnosis was less than
1 year in most cases (12 [66.7%] of 18 cases). Diagno­
sis was delayed in some patients because of the lack of
available MR imaging at the time. Among the patients
reported on after the advent of MR imaging, only 2 were
diagnosed later than 1 year. Graça et al.12 reported on a
67-year-old woman who presented with foot numbness
that was initially diagnosed as peripheral neuropathy.
The definitive tumor diagnosis was reached 2 years after
the initial symptom. Katoh et al.14 reported on a 24-year-
old woman presenting with sporadic dorsalgia. Magnetic
resonance imaging was performed 3 years later, on mani­
festation of clinical features of medullary compression.
Magnetic resonance imaging is the gold standard
for diagnosing spinal tumors. Ependymomas usually en­
hance uniformly after Gd administration.16,28 Tumor loca­
tion was distributed as follows: cervical in 2 patients, cer­
vicothoracic in 3, thoracic in 11, lumbar in 2, and multiple
3
 E. A. Iunes et al.
TABLE 1: Summary of the cases reported*

Clinical Duration of
Authors & Year Age, Sex (yrs) Features Symptoms (wks) Site Intraop WHO Grade Clinical Course Follow-Up (wks)
Cooper et al., 1951 40, F pain, MS 156 T EM/TR I† disease free 106
Cheng et al., 1996 47, F MS 34 T exo/TR myxo disease free NR
González et al., 1971 43, F MS 416 T EM/TR II disease free NR
Katoh et al., 1995 24, F pain 156 CT EMA/TR III disease free 26
Li & Holtås, 1992 NR, F NR NR L EM NR disease free NR
Oliver et al., 1981 34, F pain, MS 260 T EM III disease free 13
Wagle et al., 1988 41, F pain 52 T EMA/TR II† disease free NR
Wolfla et al., 1997 69, F pain 26 T EM/TR II† disease free 27
Duffau et al., 2000 43, F pain, MS 52 T EM/TR II disease free 106
Robles et al., 2005 47, F MS subacute T EM/TR II recurrence 98
Payer et al., 1999 62, F pain 39 T EM/TR II disease free NR
Shuurmans et al., 2006 29, F pain, MS 17 C EMA/TR III recurrence & death 106
Fuentes Rodríguez et al., 2004 47, F pain 78 L EM/TR II disease free NR
Cerase et al., 2006 56, M pain, MS 8 T EM/TR III recurrence & death 57
Graça et al., 2006 67, F MS 104 T EM/TR II recurrence 56
Hentschel et al., 2004 37, M pain, MS 17 CT exo/TR II stable disease 6
51, F pain 52 CT exo/TR II stable disease 2
Benzagmout et al., 2008 31, M pain, MS 52 C EM/TR II† recurrence NR after relapse
present case 32, M MS 4 ML EM/PR II progression & death 105

*  C = cervical; CT = cervicothoracic; EM = extramedullary; EMA = extramedullary with adhesion; exo = exophytic; L = lumbar; ML = multiple locations;
MS = medullary syndrome; myxo = myxopapillary; NR = not reported; PR = partial resection; T = thoracic; TR = total resection.
†  These grades are probable grades.

in 1 patient (present case).3,5–7,9–14,17,21,23,24,27,29,31 In contrast
to intramedullary ependymomas that clearly tend to de­
velop at the cervical medulla,19,20 the predominance of the
thoracic location was noteworthy in the present review.
Three of 5 tumors with cervical involvement extended
into the thoracic region (cervicothoracic tumors). This
observation may suggest that they might actually be cer­
vical intramedullary tumors (more prevalent) with extra­
medullary extension. The present case is the first of an
intradural extramedullary ependymoma (except for those
occurring in the conus medullaris and terminal filum)
with multiple lesions at presentation. This presentation
had been previously described in myxopapillary ependy­
momas.30
Intraoperative reports described exophytic tumors
in 3 cases (treated with total resection), extramedullary
tumors with some degree of medullary involvement in
3 cases (treated with total resection), and 13 tumors de­
scribed as exclusively extramedullary (of which 10 were
treated with total resection and 1 with partial resection;
in 2 cases the extent of resection was not specified). In the
present case, the tumor was exclusively extramedullary,
but it infiltrated the arachnoid membrane. Graça et al.12
reported a similar case of a Grade II tumor treated using
gross-total resection. The tumor presented with a “pachy­
meningitis” that might have been attributable to neoplas­
tic infiltration and contributed to the poor outcome as
observed in our patient. Finally, the true value of the sur­
geon’s intraoperative observation should be emphasized,
since minimal medullary connections or arachnoid inva­
sion might go undetected, particularly if partial resection
is considered.
Clinical improvement and local control occurred in 11
patients,6,7,9–11,14,17,21,23,29,31 5 of whom were followed up for
13–106 weeks.7,9,14,21,31 Data on follow-up were not available
for 6 patients.6,10,11,17,23,29 Two patients remained stable, al­
though the follow-up extended for only 2 and 6 weeks.13
Including the patient in the present case, recurrence or
progression occurred in 6 patients as follows:3,5,12,24,27 1
patient developed distant spinal metastasis,24 2 had local
recurrence and distant spinal metastasis,5,12 1 had local re­
currence and cerebellar metastasis,3 and 1 had spinal and
intracranial metastases.27 The patient in the present case
presented with multiple lesions at diagnosis. Three pa­
tients, including the one in the present case, died of disease
progression.5,27
Histologically, 9 ependymomas were classified as
WHO Grade II, 1 was described as myxopapillary de­
spite the thoracic location, 4 were anaplastic (Grade III),
3 were “probable” Grade II tumors, and 1 was a probable
Grade I ependymoma. The descriptions available were
not detailed for the last 4 cases.
Higher-grade gliomas are more prevalent in the ce­
rebral parenchyma, whereas lower-grade gliomas pre­
vail in the medulla.22 The present review showed a clear
predominance of low-grade ependymomas. Histological
grade does not seem to be the major determinant of clini­
cal outcome. Of the 6 cases with poor outcome,3,5,12,24,27
that is, those with recurrence or neuraxis spreading, only
2 had histological features of anaplastic ependymoma.5,27

4 J Neurosurg: Spine / December 10, 2010

Multifocal intradural extramedullary ependymoma
The 3 patients with WHO Grade II tumors with unfavor­
able outcome warrant further evaluation. The patient re­
ported by Robles et al.24 underwent gross-total resection
of an anterolateral tumor, yet the authors reported adhe­
sion to the pia mater, which does not rule out the possibil­
ity of neoplastic remnants in that area. The local recur­
rence was located in the posterior region, and histological
examination showed a Grade III ependymoma. Taking
into account that the lesion was only partially resected, a
sampling error might be inferred (the pial portion might
be a Grade III ependymoma). The patient reported on by
Graça et al.12 presented with recurrence and spinal me­
tastasis, but the tumor remained classified as a Grade II
tumor. An “important arachnoid inflammatory reaction”
was also described, which might characterize a neoplastic
infiltration and actually a partial resection, accounting for
the unfavorable outcome. The patient in the present case
also had a WHO Grade II ependymoma. The pachymen­
ingitis observed during surgery might in fact have been
tumoral infiltration that led to sampling errors. However,
the clinical feature of dissemination at presentation was
irrefutable and may also have been associated with the
unfavorable outcome. The patient described by Benzag­
mout et al.3 also had a poor outcome with cerebellar
metastasis and local recurrence. The tumor was initially
classified as a “benign ependymoma,” and the authors did
not report on the follow-up after recurrence.
Two patients with WHO Grade III ependymomas
with a favorable outcome were described by Katoh et al.14
and Oliver et al.21 However, the follow-up reported was
short (only 26 and 13 weeks, respectively).
The origin of intradural extramedullary ependy­
moma has been attributed to the presence of heterotopic
glial cells, since the earliest report by Cooper et al.7 This
observation implies the occurrence of invagination of the
neuraxis into the extramedullary space, evidenced by an
encapsulated appearance (encapsulation by pia mater and
arachnoid membrane) and absence of medullary connec­
tion. These cells evolve to a tumor within the intradural
extramedullary space. The same hypothesis has been pro­
posed to explain the origin of gliomas occurring outside
the neuraxis, including nasal and sacral gliomas.1,2,4,8,15,25,26
The presence of a medullary connection does not rule out
the hypothesis of an intramedullary tumor extending to
the extramedullary compartment. Identification of exclu­
sively extramedullary cases can be biased by subjective
interpretation and by the resolution of surgical micro­
scopes, making it difficult to rule out medullary connec­
tion. From a practical standpoint, however, all the cases
reported appeared as intradural and extramedullary le­
sions on the images, and the importance of these reports
may lie in considering ependymomas, although rare, as a
differential diagnosis of tumors at this location.
Conclusions
Intradural extramedullary ependymomas are ex­
tremely rare and predominate in women in the 5th decade
of life. Pain is the most frequent initial symptom, akin to
other tumors of the medullary canal. Magnetic resonance
imaging of the entire neuraxis is essential to rule out in­
tracranial ependymomas with metastasis to the neuraxis.
J Neurosurg: Spine / December 10, 2010
The thoracic location is the most common site for ex­
tramedullary ependymomas, unlike intramedullary ep­
endymomas, which are mostly cervical. Multifocal pre­
sentation at diagnosis had not been previously described.
The prognosis seems to be related to the extent of resec­
tion and the presence of meningeal infiltration.
Disclosure
The authors report no conflict of interest concerning the mate­
rials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript prepara­
tion include the following. Conception and design: Malheiros.
Acquisition of data: Iunes, Stávale, Pessoa. Analysis and interpreta­
tion of data: Iunes, Stávale, Pessoa, Neto. Drafting the article: Iunes,
Neto, Malheiros. Critically revising the article: Neto, Malheiros.
Reviewed final version of the manuscript and approved it for
sub­mission: all authors. Administrative/technical/material support:
Ansai, Onishi. Study supervision: Bonatelli, Cavalheiro, Neto, Mal­
heiros.
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Manuscript submitted December 8, 2009.
Accepted September 22, 2010.
Please include this information when citing this paper: published
online December 10, 2010; DOI: 10.3171/2010.9.SPINE09963.
Address correspondence to: Eduardo Augusto Iunes, M.D.,
Department of Neurology and Neurosurgery, Universidade Federal
de São Paulo, Rua Napoleão de Barros, 715/6th floor, São Paulo, SP,
Brazil, 04024002. email: eaiunes@ig.com.br.