Context.—Several distinctive mixed glioneuronal tumors that warrant recognition as clinicopathologic entities have been recently described by neuropathologists.

Objective.—To summarize important clinical, radiologic, and pathologic findings for 3 novel glioneuronal tumors (papillary glioneuronal tumor, rosetted glioneuronal tumor, and rosette-forming glioneuronal tumor of the fourth ventricle).

Data Sources.—Recent reports in the pathology literature and the authors' experience with mixed glioneuronal tumors at a major cancer center.

Conclusions.—Histologic features enabling recognition of these recently described glioneuronal tumors are presented along with remarks concerning the classification of mixed neuronal and glial tumors exhibiting unconventional appearances.

During the past decade pathologists have introduced several morphologically distinctive neoplasms to the category of mixed glioneuronal tumors. This review summarizes the clinical, imaging, and neuropathologic features of 3 neuronoglial newcomers (papillary glioneuronal tumor, rosetted glioneuronal tumor, and rosette-forming glioneuronal tumor of the fourth ventricle) and briefly addresses the problems encountered by pathologists facing difficult-to-classify brain tumors with convincing evidence of biphenotypic neuronal and glial differentiation.

The largest series and most complete description of this tumor was published by Komori et al1 in 1998, but since that time a number of case reports in the pathology literature have confirmed the initial findings,2–8 and reports with less exhaustive pathologic documentation have appeared in clinical journals.9,10 The 2000 World Health Organization (WHO) classification recognizes this low-grade tumor as a variant of ganglioglioma.11 The mean age at presentation was 27.7 years in the series of Komori et al, and reported ages range from 11 to 75 years, with males and females equally represented. Presenting symptoms have included seizures, headache, vomiting, ophthalmoparesis, and language disturbance. Rarely, a patient with this tumor is asymptomatic at the time of diagnosis. There is no association with any heritable syndrome.

This cerebral tumor is radiographically well circumscribed, may be located in any lobe (with a slight predilection for the temporal), and frequently lies near a lateral ventricle. Greatest dimension ranges from 1.5 to 7 cm. The appearance of a cystic mass with associated mural nodule is common, and contrast enhancement (sometimes ring-like) is usual. Peritumoral edema and mass effect are generally mild, and some cases are focally calcified.

Histologically, the most characteristic and striking feature of this tumor is the presence of gliovascular papillae (more accurately, pseudopapillae) composed of a hyalinized blood vessel upon which one or more layers of astrocytic cells are anchored, usually without the formation of radial, tapering cytoplasmic processes of the type seen in ependymal pseudorosettes (Figure 1). These cells lack cytologic atypia and label with glial fibrillary acidic protein (GFAP) and S100 protein, but not neuronal antigens (Figure 2). In contrast, the interpapillary space contains variable numbers of cells with neuronal nuclear features (including speckled chromatin and small nucleoli) which range in size from small, round neurocytes with clear or palely eosinophilic cytoplasm, through intermediate size “ganglioid” cells, to mature ganglion cells (Figures 3 and 4). These cells may also grow in solid sheets or nodules outside the papillary zones. Perinuclear halos in these regions may evoke oligodendroglioma, and cells with granular eosinophilic cytoplasm or minigemistocytes further this resemblance (Figure 5). Neuronal cells are often situated in either a finely fibrillar neuropil matrix or a lightly basophilic mucoid matrix and typically stain for standard neuronal markers (synaptophysin, NeuN, TU-J1; Figure 6). Scattered round cells may also stain for GFAP, and a recent report of labeling for Olig2 (a transcription factor with preferential, but not exclusive, expression in oligodendrocytes) is interesting in view of the oligodendroglioma-like appearance in these foci.12 Mitoses are rare or absent in papillary glioneural tumor (PGNT), and there have been no reports of microvascular hyperplasia or necrosis. MIB-1 proliferation indices in the series of Komori et al1 ranged from 0.5% to 2.5%, in keeping with a low-grade tumor. Nonspecific degenerative changes such as foam cell aggregation, calcification, hemosiderin deposition, and mild lymphocytic infiltration may be seen. The interface between tumor and brain tissue is reasonably sharp, but limited percolation of tumor cells into surrounding parenchyma is common.

Figure 1.

Gliovascular papillae consist of a hyalinized blood vessel covered by a monolayer of bland astrocytic cells (hematoxylin-eosin stain, original magnification ×100). Figure 2. Glial fibrillary acidic protein immunostain highlights astrocytes making up gliovascular papillae (original magnification ×100). Figure 3. Cytologic features of astrocytes in papillae (upper left) contrast with those of intermediate cells in lower right, the latter showing delicate chromatin and conspicuous nucleoli (hematoxylin-eosin stain, original magnification ×200). Figure 4. Mature ganglion cells (like that indicated by arrow) are sometimes a feature of papillary glioneural tumor (hematoxylin-eosin stain, original magnification ×200). Figure 5. Collections of clear cells simulate oligodendroglioma (hematoxylin-eosin stain, original magnification ×400). Figure 6. Synaptophysin immunostain labels interpapillary cells with neuronal differentiation (original magnification ×200).

Figure 1.

Gliovascular papillae consist of a hyalinized blood vessel covered by a monolayer of bland astrocytic cells (hematoxylin-eosin stain, original magnification ×100). Figure 2. Glial fibrillary acidic protein immunostain highlights astrocytes making up gliovascular papillae (original magnification ×100). Figure 3. Cytologic features of astrocytes in papillae (upper left) contrast with those of intermediate cells in lower right, the latter showing delicate chromatin and conspicuous nucleoli (hematoxylin-eosin stain, original magnification ×200). Figure 4. Mature ganglion cells (like that indicated by arrow) are sometimes a feature of papillary glioneural tumor (hematoxylin-eosin stain, original magnification ×200). Figure 5. Collections of clear cells simulate oligodendroglioma (hematoxylin-eosin stain, original magnification ×400). Figure 6. Synaptophysin immunostain labels interpapillary cells with neuronal differentiation (original magnification ×200).

Close modal

Ultrastructural studies have essentially supported the light microscopic and immunohistochemical findings: the cells lining gliovascular papillae show astrocytic features with cytoplasmic bundles of intermediate filaments, whereas the rounded interpapillary cells demonstrate neuronal features such as fine cytoplasmic processes containing parallel arrays of microtubules as well as cytoplasmic dense core and clear vesicles. Synaptic junctions have also been reported. Attention has been drawn to a subset of “nonspecific cells” lacking cytoplasmic specializations,1 which could represent oligodendroglial elements.12 

There is no known genetic signature for PGNT. Fluorescence in situ hybridization studies did not detect 1p deletion in any of 6 examined cases.12 A personally studied example did not manifest deletion of either chromosome 1p or 19q on loss of heterozygosity analysis. Any discussion of histogenesis is necessarily speculative, but the proximity of many tumors to the lateral ventricles raises the possibility of origin from multipotential subependymal stem cells.

The prognosis for patients with PGNT is favorable, with no reports of recurrence following gross total resection over follow-up intervals of up to 7 years.3 In summary, PGNT is a distinctive low-grade mixed glioneuronal tumor typically affecting young adults, which shares with other mixed lineage tumors (such as ganglioglioma) relative circumscription from surrounding brain, frequent presentation with seizures, and favorable prognosis following simple excision. The characteristic papillary architecture and bipartite (astrocytic and neuronal/neurocytic) cell populations distinguish this lesion from other tumors with which it shares histologic features such as dysembryoplastic neuroepithelial tumor, extraventricular neurocytoma, pilocytic astrocytoma, oligodendroglioma, and astroblastoma.

This tumor was described by one of us (M.K.R.) in a 1999 report from Memorial Sloan-Kettering Cancer Center detailing a series of diffusely infiltrating brain tumors of adulthood exhibiting predominantly astrocytic morphology, but containing distinctive neuropil-like islands in which the constituent cells tended to form rosettes.13 Fundamental differences from PGNT include a diffusely infiltrating growth pattern, absence of papillary gliovascular structuring, and a far less favorable prognosis. Since its initial description, a handful of additional case reports have appeared in the literature.14–16 

The cases reported to date have been clinically and radiologically indistinguishable from diffuse gliomas, all except one intramedullary spinal example14 involving cerebral hemispheres (including deep white matter, cortex, and deep gray structures). Patients with intracranial tumors have presented with seizures, focal neurologic deficits, or signs of increased intracranial pressure; the single intraspinal (cervicothoracic) tumor was associated with hemiparesis and unilateral sensory loss. Neuroimaging studies at presentation usually show one or more cerebral lobes involved by a T1-hypointense, T2-hyperintense mass with variable mass effect and edema (findings all common for diffuse glioma; Figure 7). Contrast enhancement, usually minimal at diagnosis, may become conspicuous with tumor progression. There has been no association with any genetic syndrome.

Figure 7.

Axial T2-weighted magnetic resonance imaging of rosetted glioneuronal tumor showing a large, heterogeneously hyperintense parieto-occipital mass. (Courtesy of Dr Michael Deck, New York Presbyterian Hospital, New York, NY)

Figure 7.

Axial T2-weighted magnetic resonance imaging of rosetted glioneuronal tumor showing a large, heterogeneously hyperintense parieto-occipital mass. (Courtesy of Dr Michael Deck, New York Presbyterian Hospital, New York, NY)

Close modal

The histologic findings closely resemble diffuse astrocytoma and often feature dominating fibrillary, gemistocytic, or protoplasmic elements. Exceptionally, diffuse components raising question of oligodendroglioma may be encountered. Atypical astrocytic cells freely infiltrate normal structures including cerebral cortex. Mitoses may be seen, but microvascular proliferation and necrosis are not usually evident; astrocytic elements would correspond to WHO grade 2 or 3 astrocytoma (Figure 8). Unlike diffuse astrocytoma, rosetted glioneural tumor (RGNT) shows relatively abrupt transition between its coarsely fibrillary or gemistocytic astroglial components and round or ovoid islands having a more finely fibrillar, neuropil-like quality (Figure 9). Inhabiting these islands are variable numbers of rounded neurocytic cells (sometimes with perinuclear halos) which may be preferentially located at the periphery, where they form linear arcs or rosettes (the largest of which resemble pineocytomatous rosettes). Mature ganglion cells which lack atypical features may also be present. Although these islands (which can measure hundreds of micrometers in diameter) are well delineated from the surrounding sea of astrocytic elements, they may be quite inconspicuous and are easily overlooked. Although the islands are most often hypocellular compared to the surrounding gliomatous tissue, an example with hypercellular islands has been reported.16 As one might expect, the neuropil islands are distinguished by strong immunostaining for synaptophysin, and nuclei of cells embedded in the islands may show reactivity for neuN and anti-Hu (Figures 10 and 11). The astrocytic component shows labeling for GFAP and may also stain for p53; GFAP-positive astrocytes may occasionally appear stranded in the neuropil islands. MIB-1 proliferation index is variable, ranging from 1.0% to 18.1%, the latter value seen in a recurrence. Although MIB-1 labeling may be virtually restricted to astrocytic cells, neuropil islands may also show staining and can exhibit proliferation indices exceeding those of astrocytic components.

Figure 8.

Large fields of rosetted glioneural tumor are indistinguishable from diffuse astrocytoma (hematoxylin-eosin stain, original magnification ×100). Figure 9. Neuropil island with compact, finely fibrillar matrix; constituent cells possess rounded nuclei and clear cytoplasm, and form ill-defined rosettes (hematoxylin-eosin stain, original magnification ×100). Figure 10. Immunostain for synaptophysin strongly labels neuropil islands in rosetted glioneural tumor (original magnification ×100). Figure 11. NeuN immunostain frequently labels a subset of cells making up neuropil islands (synaptophysin immunostain, original magnification ×100).

Figure 8.

Large fields of rosetted glioneural tumor are indistinguishable from diffuse astrocytoma (hematoxylin-eosin stain, original magnification ×100). Figure 9. Neuropil island with compact, finely fibrillar matrix; constituent cells possess rounded nuclei and clear cytoplasm, and form ill-defined rosettes (hematoxylin-eosin stain, original magnification ×100). Figure 10. Immunostain for synaptophysin strongly labels neuropil islands in rosetted glioneural tumor (original magnification ×100). Figure 11. NeuN immunostain frequently labels a subset of cells making up neuropil islands (synaptophysin immunostain, original magnification ×100).

Close modal

Little is known about the genetics of RGNT, but one case studied by comparative genomic hybridization showed a gain of 7q and loss of 9p (findings seen in diffuse astrocytoma). Reverse transcriptase polymerase chain reaction assays for 1p and 19q performed at our institution have not detected major codeletions of the sort observed in oligodendroglial tumors.17 These findings and the predominantly astroglial appearance of most tumors raise the possibility that RGNT may represent a variant of diffuse astrocytoma with aberrant neuronal differentiation.

Although brain tumors with neuronal differentiation frequently have a relatively favorable prognosis, this principle does not seem applicable to RGNT, as most cases with sufficient follow-up have shown evidence of tumor progression (including leptomeningeal spread in the spinal cord example), and death due to disease has been recorded. Studies of larger numbers of cases may uncover prognostic factors peculiar to this entity, but for now the tumor should be considered potentially aggressive. Even examples of apparently low histologic grade may behave in a malignant fashion.

Following their initial report in 1998, Komori et al18 published a detailed description of this tumor in 200219 based on a series of 11 cases seen in consultation at The Mayo Clinic, and this has been followed by case reports of identical lesions.20,21 Two cases previously reported as “dysembryoplastic neuroepithelial tumor of the cerebellum” appear to represent examples of this tumor.22,23 A unifying feature of this entity has been involvement of fourth ventricle or aqueduct. Although a consistent site of origin has been difficult to pinpoint, most tumors have at least focally involved cerebellum. Patients have mostly been young adults, and ages have ranged from 12 to 59 years. Presenting symptoms have varied in duration from days to 13 years and are typical of an intraventricular posterior fossa tumor, with headache and ataxia reported most often; 3 tumors have been discovered incidentally, and 1 example was associated with a left fourth cranial nerve palsy.

Imaging studies have revealed midline masses occupying the fourth ventricle or cerebral aqueduct and commonly involving cerebellum (especially vermis) with a cerebellar attachment demonstrable at surgery for most tumors in the original series of Komori et al. There is often involvement of surrounding periventricular and periaqueductal tissue such as dorsal pons, midbrain, thalamus, or pineal region, and multinodularity or multicentricity may be observed. Tumors are relatively circumscribed and often partially cystic by magnetic resonance imaging, with the majority showing heterogeneous contrast enhancement.

Two tissue types are evident histologically. The first is a cytologically bland and generally paucicellular astroglial proliferation with spindle, stellate, and piloid cells resembling pilocytic astrocytoma (Figure 12). The most hypocellular examples of this glial component may suggest reactive piloid gliosis, but other cases show a level of cellularity and architectural patterns that are incompatible with a reactive process. Eosinophilic granular bodies, Rosenthal fibers, hyalinized blood vessels, and microcystic change may further foster a false impression of pilocytic astrocytoma for the unwary pathologist. The clue to correct diagnosis lies in the second component, in which cells with small, round, regular nuclei and speckled chromatin form perivascular pseudorosettes and miniature neurocytic rosettes with a delicate neuropil matrix (Figure 13). Longitudinal sectioning may reveal perivascular columns of cells, frequently separated by mucoid matrix, mimicking dysembryoplastic neuroepithelial tumor (DNT). The specific glioneuronal element of DNT may also be suggested by patternless sheets of nondescript oligodendroglia-like cells (Figure 14). Scattered dysmorphic ganglion cells are seen in some tumors. Notably absent are significant cytologic atypia and mitotic activity, but glomeruloid capillaries of the type seen in pilocytic astrocytoma may be encountered.

Figure 12.

Hypocellular glial foci with spindle cells and hyalinized blood vessels resemble pilocytic astrocytoma (hematoxylin-eosin stain, original magnification ×100). Figure 13. Rosettes resembling those of Homer-Wright or neurocytic type (hematoxylin-eosin stain, original magnification ×400). Figure 14. Sheets of oligodendrocyte-like cells separated by collections of mucin in an alveolar pattern simulate dysembryoplastic neuroepithelial tumor (hematoxylin-eosin stain, original magnification ×100). Figure 15. Synaptophysin labeling of neuropil rosettes (original magnification ×200).

Figure 12.

Hypocellular glial foci with spindle cells and hyalinized blood vessels resemble pilocytic astrocytoma (hematoxylin-eosin stain, original magnification ×100). Figure 13. Rosettes resembling those of Homer-Wright or neurocytic type (hematoxylin-eosin stain, original magnification ×400). Figure 14. Sheets of oligodendrocyte-like cells separated by collections of mucin in an alveolar pattern simulate dysembryoplastic neuroepithelial tumor (hematoxylin-eosin stain, original magnification ×100). Figure 15. Synaptophysin labeling of neuropil rosettes (original magnification ×200).

Close modal

Immunostain for synaptophysin reliably labels the neuropil matrix of neurocytic and perivascular pseudorosettes as well as the cytoplasm of their constituent cells (Figure 15). MAP-2 and neuron-specific enolase reactivity parallel that of synaptophysin, whereas staining for NeuN was not detected in 1 recent case. In contrast, GFAP and S100 protein staining characterize the astrocytic (but not the neurocytic) elements, and oligodendroglia-like cells may stain only for S100 protein. Ultrastructural studies have confirmed the presence of 2 cellular elements with a glial component demonstrating cytoplasmic bundles of intermediate filaments and a neuronally differentiated component showing cytoplasmic processes with longitudinally arranged microtubules, dense core granules, and in some cases, synapses.19 

The indolent nature of this tumor is evidenced by the absence of aggressive histologic features, frequently long preoperative history, low MIB-1 proliferation indices (ranging from 0.35% to 3.07% in the original series), and relatively favorable prognosis. Although one patient developed a ring enhancing brain stem lesion after radiotherapy and ultimately died, death from progressive tumor seems to be rare. Because of the close proximity to vital brain stem structures in many cases, complete excision is either impossible or results in postoperative deficits (such as 6th and 7th cranial nerve palsies), and extended follow-up will be necessary to determine optimum therapy for patients with residual disease. Although there are similarities between rosetted glioneuronal tumor of the fourth ventricle and DNT, these are perhaps outnumbered by differences. Whereas DNT is typically a supratentorial, multinodular, and intracortical tumor in children or young adults with seizures and no neurologic deficit,24 rosetted glioneuronal tumor of the fourth ventricle is an infratentorial, intraventricular mass lesion affecting a slightly older age group which presents with signs of ventricular obstruction and which may cause focal deficits. Furthermore, whereas rosettes may be seen in DNT, they typically lack the well-developed neurocytic differentiation and synaptophysin positivity of rosetted glioneuronal tumor of the fourth ventricle.

The category of mixed glial and neuronal tumors represents a vast and largely uncharted territory which is ripe for exploration. Noteworthy in this regard is a recent study by Perry et al25 of oligodendrogliomas with neurocytic differentiation. The 4 cases in this report showed areas of typical infiltrating oligodendroglioma and separate, morphologically distinct regions with neurocytic features including Homer-Wright and perivascular rosettes which stained for synaptophysin. Three of the cases showed 1p and 19q codeletions typical of oligodendroglioma, raising some intriguing questions about the appropriate nomenclature for such lesions and about the histogenesis of oligodendroglioma in general. Reports of action potential generation by cultured oligodendroglioma cells,26 of oligodendrogliomas showing immunopositivity for various neuronal antigens,27 and expressing genes associated with neuronal functions28 have raised questions about a possible common lineage for neurons and oligodendrocytes, and the existence of such combined tumors could be interpreted as support for this idea. Whether these examples of composite oligodendroglioma/neurocytoma represent instances of aberrant neuronal differentiation in a glioma or evidence of neoplasia in a multipotent stem cell is unclear.

The practical problem of classifying mixed glioneuronal neoplasms extends beyond recognition of distinctive examples such as those described above. Pathologists may occasionally encounter cases of histologically typical glioblastoma which show limited immunostaining for a single neuronal marker, usually synaptophysin. In this setting, there is no convincing evidence to suggest that such tumors will behave differently from conventional glioblastoma, and designation of such lesions as mixed glioneuronal neoplasms is not justified in our view. However, there are occasional tumors which combine high-grade astrocytic elements with small cell components that label for neuronal antigens and which also show ultrastructural evidence of neuronal differentiation. Separation of such tumors from conventional glioblastoma may be worthwhile, especially given that some examples show clinical progression more akin to small cell embryonal tumors with cerebrospinal fluid dissemination.29 These and other mixed neuronoglial tumors currently defy precise subclassification. For instance, one occasionally encounters examples of clearly anaplastic tumors with histologic mixtures of neoplastic neuronal, neurocytic, and astrocytic forms in various proportions. Such tumors are not accommodated in the current WHO classification scheme, and our practice has been to assign such unclassifiable cases the descriptive designation “malignant mixed glioneuronal tumor” with an estimate of histologic grade based on conventional features such as mitotic activity and necrosis. We reserve the term anaplastic ganglioglioma for those rare overtly anaplastic tumors with features of conventional ganglioglioma which include relative circumscription, eosinophilic granular bodies, perivascular chronic inflammation, and a reticulin-rich nested architectural pattern. This noncommittal approach has the advantage of acknowledging the limitations on our current knowledge of how to classify neuronoglial tumors.

Komori
,
T.
,
B. W.
Scheithauer
, and
D. C.
Anthony
.
et al
.
Papillary glioneuronal tumor: a new variant of mixed neuronal-glial neoplasm.
Am J Surg Pathol
1998
.
22
:
1171
1183
.
Prayson
,
R. A.
Papillary glioneuronal tumor.
Arch Pathol Lab Med
2000
.
124
:
1820
1823
.
Bouvier-Labit
,
C.
,
L.
Daniel
,
H.
Dufour
,
F.
Grisoli
, and
D.
Figarella-Branger
.
Papillary glioneuronal tumor: clinicopathological and biochemical study of one case with 7-year follow up.
Acta Neuropathol
2000
.
99
:
321
326
.
Broholm
,
H.
,
F. F.
Madsen
,
A. A.
Wagner
, and
H.
Laursen
.
Papillary glioneuronal tumor: a new tumor entity.
Clin Neuropathol
2002
.
21
:
1
4
.
Tsukayama
,
C.
and
Y.
Arakawa
.
A papillary glioneuronal tumor arising in an elderly woman: a case report.
Brain Tumor Pathol
2002
.
19
:
35
39
.
Kordek
,
R.
,
R.
Hennig
,
E.
Jacobsen
, and
M.
Kearney
.
Papillary glioneuronal tumor: a new variant of benign mixed brain neoplasm.
Polish J Pathol
2003
.
54
:
75
78
.
Lamszus
,
K.
,
M.
Makrigeorgi-Butera
,
R.
Laas
,
M.
Westphal
, and
D.
Stavrou
.
24-year-old female with a 6-month history of seizures.
Brain Pathol
2003
.
13
:
115
116
.
Kim
,
D. H.
and
Y-L.
Suh
.
Pseudopapillary neurocytoma of temporal lobe with glial differentiation.
Acta Neuropathol
1997
.
94
:
187
191
.
Borges
,
G.
,
L.
Bonilha
, and
A. S.
Menezes
.
et al
.
Long term follow-up in a patient with papillary glioneuronal tumor.
Arq Neuropsiquitr
2004
.
62
:(
3-B
).
869
872
.
Stosic-Opincal
,
T.
,
V.
Peric
,
S.
Gavrilovic
,
M.
Gavrilovic
,
Z.
Markovic
, and
R. M.
Sener
.
Papillary glioneuronal tumor.
Am J Roentgenol
2005
.
185
:
265
267
.
Kleihues
,
P.
and
W. K.
Cavenee
.
eds
.
Pathology and Genetics of Tumours of the Central Nervous System.
Lyon, France: IARC Press; 2000. World Health Organization Classification of Tumours.
.
Tanaka
,
Y.
,
H.
Yokoo
, and
T.
Komori
.
et al
.
A distinct pattern of Olig2-positive cellular distribution in papillary glioneuronal tumors: a manifestation of the oligodendroglial phenotype?
Acta Neuropathol
2005
.
110
:
39
47
.
Teo
,
J. G. C.
,
S. H.
Gultekin
,
M.
Bilsky
,
P.
Gutin
, and
M. K.
Rosenblum
.
A distinctive glioneuronal tumor of the adult cerebrum with neuropil-like (including “rosetted”) islands: a report of 4 cases.
Am J Surg Pathol
1999
.
23
:
502
510
.
Harris
,
B. T.
and
D. S.
Horoupian
.
Spinal cord glioneuronal tumor with “rosetted” neuropil islands and meningeal dissemination: a case report.
Acta Neuropathol
2000
.
100
:
575
579
.
Prayson
,
R. A.
and
C. M.
Abramovich
.
Glioneuronal tumor with neuropil-like islands.
Hum Pathol
2000
.
31
:
1435
1438
.
Keyvani
,
K.
,
C. H.
Rickert
,
K.
von Wild
, and
W.
Paulus
.
Rosetted glioneuronal tumor: a case with proliferating neuronal nodules.
Acta Neuropathol
2001
.
101
:
525
528
.
Barbashina
,
V.
,
P. A.
Salazar
,
M.
Ladanyi
, and
M. K.
Rosenblum
.
Glioneuronal tumor with neuropil-like islands (GTNI): a report of 8 cases with chromosome 1p/19q deletion analysis.
Am J Surg Pathol
2007
.
In press
.
Komori
,
T.
,
B. W.
Scheithauer
, and
J.
Sung
.
Rosette-forming mixed neuronal-glial tumor in the fourth ventricle [abstract].
J Neuropathol Exp Neurol
1998
.
57
:
520
.
Komori
,
T.
,
B. W.
Scheithauer
, and
T.
Hirose
.
A rosette-forming glioneuronal tumor of the fourth ventricle: infratentorial form of dysembryoplastic neuroepithelial tumor?
Am J Surg Pathol
2002
.
25
:
582
591
.
Preusser
,
M.
,
W.
Dietrich
,
T.
Czech
,
D.
Prayer
,
H.
Budka
, and
J. A.
Hainfellner
.
Rosette-forming glioneuronal tumor of the fourth ventricle.
Acta Neuropathol
2003
.
106
:
506
508
.
Adachi
,
J.
,
R.
Nishikawa
,
T.
Hirose
, and
M.
Matsutani
.
Mixed neuronal-glial tumor of the fourth ventricle and successful treatment of postoperative mutism with bromocriptine: case report.
Surg Neurol
2005
.
63
:
375
379
.
Yamane
,
Y.
,
J.
Hirato
, and
A.
Sasaki
.
et al
.
Dysembryoplastic neuroepithelial tumor of the cerebellum [abstract in Japanese].
Brain Tumor Pathol
2000
.
17
:(
suppl 1
).
86
.
Kuchelmeister
,
K.
,
T.
Demirel
,
E.
Schlorer
,
M.
Bergmann
, and
F.
Gullotta
.
Dysembryoplastic neuroepithelial tumor of the cerebellum.
Acta Neuropathol
1995
.
89
:
385
390
.
Daumas-Duport
,
C.
,
B. W.
Scheithauer
,
J-P.
Chodkiewicz
,
E. R. Jr
Laws
, and
C.
Vedrenne
.
Dysembryoplastic neuroepithelial tumor: a surgically curable tumor of young patients with intractable partial seizures: report of thirty-nine cases.
Neurosurgery
1988
.
23
:
545
556
.
Perry
,
A.
,
B. W.
Scheithauer
,
R. J. B.
Macaulay
,
C.
Raffel
,
K. A.
Roth
, and
J. M.
Kros
.
Oligodendrogliomas with neurocytic differentiation: a report of 4 cases with diagnostic and histogenetic implications.
J Neuropathol Exp Neurol
2002
.
61
:
947
955
.
Patt
,
S.
,
C.
Labrakakis
, and
M.
Bernstein
.
et al
.
Neuron-like physiological properties of cells from human oligodendroglial tumors.
Neuroscience
1996
.
71
:
601
611
.
Wolf
,
H. K.
,
R.
Buseli
,
I.
Blumcke
,
O. D.
Wiestler
, and
T.
Pietsch
.
Neural antigens in oligodendrogliomas and dysembryoplastic neuroepithelial tumors.
Acta Neuropathol
1997
.
94
:
436
443
.
Mukasa
,
A.
,
K.
Ueki
, and
X.
Ge
.
et al
.
Selective expression of a subset of neuronal genes in oligodendroglioma with chromosome 1p loss.
Brain Pathol
2004
.
14
:
34
42
.
McLendon
,
R. E.
,
R. C.
Bentley
, and
J. E.
Parisi
.
et al
.
Malignant supratentorial glial-neuronal neoplasms: report of two cases and review of the literature.
Arch Pathol Lab Med
1997
.
121
:
485
492
.

The authors have no relevant financial interest in the products or companies described in this article.

Author notes

Reprints: Mark A. Edgar, MD, Department of Pathology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021 ([email protected])