Papillary Tumor of the Pineal Region: Two Case Studies and a Review of the Literature
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1 Available online at Annals of Clinical & Laboratory Science, vol. 41, no. 2, 2011 Papillary Tumor of the Pineal Region: Two Case Studies and a Review of the Literature Kyle A Rickard 1, John R Parker 1,2, Todd W Vitaz 2, Alexis R Plaga 2, Stephanie Wagner 2, Joseph C Parker, Jr 1 1 University of Louisville Department of Pathology; 2 Norton Neuroscience Institute Abstract. Papillary tumor of the pineal region (PTPR) is a newly recognized distinct entity in the 2007 World Health Organization nomenclature. This tumor is characterized by epithelial-appearing areas with papillary features and more densely cellular areas that often display ependymal-like differentiation. Ultrastructurally, this rare neuroepithelial tumor possesses neuroendocrine, secretory, and ependymal organelles that likely originate from the subcommissural organ (SCO) near the aqueduct of Sylvius. To date, approximately fifty-seven described cases worldwide have been recognized, with ages ranging from 5 years to 66 years (mean age=32 years). Clinical presentation most often includes headache and obstructive hydrocephalus. The tumor, which is well circumscribed, may be cystic and radiographically is often considered to be consistent with the findings of a pineocytoma. Microscopic evaluation often demonstrates a lesion with papillary areas lined by epithelioid tumor cells with eosinophilic cytoplasm and more cellular areas with cells exhibiting clear or vacuolated cytoplasm. Perivascular and true rosettes may be identified. Distinctive immunohistochemical features including reactivity for keratins (AE1/AE3, CAM 5.2, CK18) and only focal GFAP staining help distinguish this neoplasm from an ependymoma. The relative paucity of data compiled for this tumor makes giving an accurate diagnosis and prognosis a daunting task. We discuss two additional cases of PTPR that presented to us within a three-month span in order to more fully elucidate the possible presentations of this rare entity. Furthermore, we examine now 59 reported cases of PTPR in order to review the current diagnostic and treatment modalities in addition to exploring emerging research encompassing this unusual neoplasm. Keywords: papillary tumor of the pineal region, subcommissural organ, papillary neoplasm, PTPR Introduction Papillary tumor of the pineal region (PTPR) is a newly recognized distinct entity in the 2007 World Health Organization nomenclature. Currently, this rare neuroepithelial tumor is thought to possibly arise from the specialized ependyma of the subcommisural organ (SCO). Microscopic evaluation often demonstrates a lesion with atypical small and intermediate size epithelioid tumor cells with eosinophilic cytoplasm found in perivascular clusters in a papillary pattern and sheets. Address correspondence and reprint requests to John R. Parker, Department of Pathology, University of Louisville, 530 South Jackson St., Louisville, KY 40202; tel (502) ; fax (502) ; j0park09@louisville.edu Immunohistochemical stains include reactivity for keratins (AE1/AE3, CAM 5.2, CK18) in the papillary structures, but only focal GFAP staining. We discuss two cases of PTPR that presented to us within a three-month span as well as examine the other 57 cases identified in the literature in order to more fully elucidate the possible presentations of this rare entity. Materials and Methods After the initial diagnosis was made through hematoxylin and eosin evaluation of the tumors, the following immunohistochemical stains were performed on permanent sections. In our first case, we utilized cytokeratin 18 (CK18, 1:50, Dako, Carpentaria, Calif.), CAM 5.2 (1:50, BD /11/ by the Association of Clinical Scientists, Inc.
2 Biosciences, San Jose, Calif.), AE1/AE3 (1:100, Dako, Carpentaria, Calif.), neuron specific enolase (NSE, 1:150, Zymed, Carlsbad, Calif.), synaptophysin (1:300, Dako, Carpentaria, Calif.), S-100 protein (1:800, Dako, Carpentaria, Calif.), glial fibrillary acidic protein (GFAP, RTU [Ready To Use], Leica, Bannockburn, Ill.), vimentin (1:100, Dako, Carpentaria, Calif.), epithelial membrane antigen (EMA, RTU, Leica, Bannockburn, Ill.), p53 (RTU, Leica, Bannockburn, Ill.), and MIB-1 (1:50, Dako, Carpentaria, Calif.) In the second case, the aforementioned stains were deployed with the exception of AE1/AE3, S100, EMA, and vimentin. We added the immunohistochemical stain chromogranin (1:100, Zymed, Carlsbad, Calif.) in our second case. The dilutions used are proprietary and are not stated in the literature. Papillary Tumor of the Pineal Region 175 Fig 1. Axial T1 weighted MRI image at 1.7 mm slices, post contrast. 48-year-old male, heterogenous enhancing mass in the pineal gland region with satellite nodule (arrow). Case Reports First Case In our first case, a previously healthy 48-year-old man presented in January 2008 with a two-month history of increasingly severe headaches along with memory loss. MRI of his brain with contrast demonstrated a heterogeneously enhancing 1.1 X 1.3 X 1.4 cm mass in the pineal region along with a 0.8 cm satellite nodule, consistent with a primary pineal tumor. The mass extended into the third ventricle and caused obstructive hydrocephalus. The patient underwent endoscopic third ventriculostomy; however, biopsy of the tumor was not performed because of poor visualization. The patient was lost to follow-up, but presented six months later with complaints of worsening headaches, short-term memory problems, and ataxia. Repeat cranial imaging showed progression of the pineal region lesion now 2.1 x 1.9 x 1.8 cm (Figure 1). He underwent successful endoscopic biopsy, and microscopic analysis of the tumor revealed a papillary to pseudopapillary epithelialappearing tumor (Figure 2) that possessed ependymal-like differentiation with perivascular rosettes and rare true rosettes. Mitoses were less than five per 10 high power fields, and isolated necrotic foci were observed. Mildly pleomorphic tumor nuclei were noted throughout the mass. Fig 2. Hemotoxylin and Eosin stain in PTPR of 48-year-old man (200X). PAS with diastase highlighted vessels in perivascular rosettes. No neuroblastic rosettes were recognized. The neoplasm was moderately to strongly decorated with cytokeratin 18 (Figure 3), neuron specific enolase (NSE), S-100, glial fibrillary acidic protein (GFAP), and vimentin. CAM 5.2 displayed focally weak decoration. In addition, epithelial membrane antigen (EMA), synaptophysin, and AE1/AE3 either failed to stain or weakly marked the tumor. The p53 immunostain diffusely decorated the tumor; the visually estimated MIB-1 nuclear staining was 15% to 20%. Overall, this tumor exhibited the features described in the Fèvre Montange et al. retrospective study of 31 cases of this entity [1].
3 176 Annals of Clinical & Laboratory Science, vol. 41, no. 2, 2011 Fig 3. CK18 positive immunostaining in PTPR of 48-year-old man (600X). Following the diagnosis, the patient underwent surgical gross-total resection of his lesion via suboccipital supracerebellar approach. After the operation, the patient developed superior gaze palsy, double vision, and fatigue. He was discharged to inpatient rehabilitation with partial resolution of these alterations. He was treated with postoperative fractionated radiation 54 Gy followed by 12 cycles of chemotherapy with temozolamide and etoposide. At his last followup (14 months), his imaging failed to show any evidence of recurrence. The visual dysfunction had resolved, and his only complaints were that of fatigue and short-term memory dysfunction, both of which were gradually improving. cells with eosinophilic cytoplasm found in sheets and perivascular clusters in a papillary and pseudopapillary pattern (Figure 5). Perivascular and true rosettes were identified in the neoplasm. Mitotic activity was not prominent (less than 1 per 10 high power fields); however, mild to moderate nuclear pleomorphism was evident. No necrosis was seen. The immunochemical panel obtained showed strong positivity for NSE, CAM 5.2 (Figure 6) and cytokeratin 18 (CK18), with focal positivity for chromogranin, synaptophysin and p53. In this case, chromogranin was repeated; in both instances focal positivity was noted. The MIB-1 cell cycle labeling was visually estimated and varied from 2% to 15% throughout the lesion. The negative reaction of GFAP and strongly positive cytokeratin CK18 was also consistent with PTPR [2, 3]. Second Case Our second case represented a 36-year-old woman who presented with a one-month history of increasingly severe occipital headaches. The days prior to her evaluation, the patient noticed increased visual blurriness along with intermittent diplopia and ataxic gait. MRI of her brain displayed a 1.8 cm lesion originating in her pineal gland region, consistent with a pineal tumor (Figure 4). In addition, significant hydrocephalus was apparent with associated tonsillar herniation through the foramen magnum. The patient underwent endoscopic third ventriculostomy to treat the hydrocephalus with concurrent endoscopic tumor biopsy. Microscopic evaluation demonstrated a lesion with atypical intermediate size epithelioid tumor Fig 4. Axial T1 weighted MRI image at 1.7 mm slices, post contrast. 36-year-old female, heterogenously enhancing mass in pineal gland region with hydrocephalus and obstruction of the cerebral aqueduct. Fig 5. Hemotoxylin and Eosin stain in PTPR of 36-year-old woman (100X).
4 Papillary Tumor of the Pineal Region 177 surgery, radiotherapy, or chemotherapy is used alone or in conjunction [4, 20]. Fig 6. CAM5.2 postitive immunostaining in PTPR of 36-yearold woman (200X). The patient underwent a gross-total surgical resection of her pineal mass via a suboccipital supracerebellar approach. She tolerated the procedure well, with the exception of a new postoperative superior gaze palsy, which eventually partially resolved. She was then treated with concurrent fractionated radiation plus temozolamide (45 Gy), followed by six cycles of temozolamide. At last follow-up, the patient was 18 months from her initial diagnosis and was doing well, save for mild visual disturbances associated with fatigue. Her imaging studies at that time failed to show any sign of recurrence. Discussion The evolution in the classification of pineal tumors has led to the emergence of PTPR. Based on a series of six tumors with identical histological features, PTPR was first described as a distinct entity in 2003 [4]. To date, there are now 59 reported cases, including six cases in children under the age of 16 years (10.2%) [1, 5-19]. PTPR generally presents with non-specific symptoms, including headache and visual disturbances due to obstructive hydrocephalus [20]. Neuroimaging usually displays a large (2-4 cm), well-circumscribed contrast enhancing tumor, which occasionally has cystic elements [8, 21]. Previous MRI literature has reported a heterogeneously enhancing mass in the pineal region [4, 10]. PTPR is prone to local recurrence, whether Histopathologically, both of our tumors displayed distinctive features described for PTPR. This tumor is an epithelial-appearing lesion with focal papillary architecture, as well as other densely cellular areas that show ependymallike differentiation. Within the cellular areas, true rosettes and tubules are often identified, consisting of cells with a clear or vacuolated cytoplasm. Occasionally, PAS positive islands may be found. Nuclei are round to oval with stippled chromatin. In the papillary sites, vessels are layered with large, pale to eosinophilic columnar cells. While microvascular proliferation is usually absent, vessels are often hyalinized. Mitotic activity is reported to vary from 0 to 10 per 10 HPF, and necrotic foci may be identified. There is usually a clear demarcation between the tumor and the residual normal pineal gland [20]. PTPR is now viewed as a separate entity from choroid plexus papilloma and ependymoma, although there is significant overlap [20]. PTPR displays prominent decoration with cytokeratins, which are most characteristically seen in papillary structures. CK18 is the cytokeratin most often associated with PTPR, although KL1, AE1/ AE3, and CAM 5.2 also commonly decorate these tumors. Due to the rarity of PTPRs, no set positive or negative cutoffs have been established for these markers [20]. In PTPR, staining is also seen with NSE and S-100. Focal decoration with chromogranin, synaptophysin, and EMA is also described. In contrast to the strong GFAP decorations in ependymomas, GFAP immunoreactivity in PTPR is usually focal or absent [10, 13]. Choroid plexus tumors frequently stain for membranous Kir 7.1 or cytoplasmic stanniocalcin-1; however, these two markers are absent in the majority of PTPR [20]. Transthyretin is more often expressed in choroid plexus tumors as well. Although larger biopsies should display the morphological features of PTPR, small, limited biopsies may fail to show
5 178 Annals of Clinical & Laboratory Science, vol. 41, no. 2, 2011 enough detail to differentiate PTPR from pineocytomas or pineoblastomas. In these cases, immunohistochemistry remains an invaluable tool. Strong immunoreactivity to synaptophysin and absent pankeratin and CK18 staining should help favor pineocytoma/pineoblastoma over PTPR. NFP is often reactive in these two neoplasms, but is not typically seen in PTPR. In addition, retinal S-antigen and/or rhodopsin positivity associated with photosensory differentiation should favor either pineocytoma or pineoblastoma in this location [20]. The remnants of the specialized ependymal cells of the subcommissural organ (SCO) are currently thought to give rise to the neoplastic cells of PTPR. The SCO, which is a part of the circumventricular organs (CVO), relays information as transducers between the blood, neurons, and the cerebrospinal fluid [12, 22]. The SCO reaches its zenith in embryonic life; afterwards it regresses to leave only traces of the cells in adults [22]. In conclusion, both of our cases stained with cytokeratins, in particular CK18. NSE was also positive in both patients. Vimentin, AE1/AE3, and S-100 immunohistochemical stains were not performed on the second case; however, the panel of markers performed, in conjunction with the morphology, was sufficient to render the diagnosis. Antibody decorations for the other markers were variable, which is often seen in PTPR [20]. Interestingly, our first lesion initially displayed moderate GFAP positivity. Repeat testing was negative for GFAP, strengthening the diagnosis of PTPR. The prognosis of PTPR is uncertain. These tumors are characterized by frequent local recurrence, and thus the literature currently suggests they may be graded either II or III [20], but complete criteria for grading are not yet formulated. In a series of 31 cases reviewed by Fèvre-Montange et al, progression was identified in 72% of cases, with five-year estimates of overall and progressionfree survival set at 73% and 27%, respectively. Incomplete resection and a mitotic index higher than five per 10 high power fields correlated with decreased survival and increased recurrence. Gross total resection was the only clinical factor strongly associated with overall survival and recurrence, but the results were not statistically significant [1]. Because of the few reported cases of PTPR, there are no current standard treatment options beyond gross total resection. Fifteen patients in the 2006 Fèvre-Montange study [1] received radiation therapy; nine after complete resection and six after incomplete resection. It is difficult to further delineate their results, considering the patients also received different therapeutic modalities. At the time, they remarked that further studies are needed for a better understanding of the behavior of this tumor and to determine the ideal postoperative treatment, including radiotherapy and chemotherapy. Subsequent authors have echoed this assertion [7, 9]. Unfortunately, examination of the current literature reveals no consensus regarding the best management for PTPR patients. Of the 59 cases examined, 56 described treatment modalities (Table 1). Surgery was used alone in 13 of 56 cases (23.2%), while surgery and radiotherapy were employed in 24 of 56 cases (42.9%). Surgery plus radiotherapy and chemotherapy was the preferred treatment plan for 30.3% of the patients (17 of 56). Radiotherapy was used in one case where surgery was contraindicated [18], and radiotherapy was used in conjunction with chemotherapy when the patient had extensive dissemination [15]. Since the publication of the 2007 WHO guidelines, the number of reported cases of PTPR has almost doubled [20]. Since neuropathologists are now aware of this entity and have firmly placed it into their differential list of tumors in the pineal region, the number will grow in the coming years. Although this tumor will remain uncommon, hopefully enough information will be acquired to better understand effective treatment modalities beyond the current unproven regimens. Another uncertainty is the role that mitotic activity or MIB-1 proliferative indices have in the progression or recurrence of the tumor. In our first case, the MIB-1 index was 15% to 20%, which was the highest of any of the 59 reported cases. This tumor was aggressive, with extensive
6 Table 1. Review of Clinical and Histological Data from 59 reported cases of PTPR. Papillary Tumor of the Pineal Region 179 Source Case Age Size (cm) Therapy 1 Necrosis Mitoses 2 MIB-1 Recurrence Follow-up (Years)/Sex Percentage (months) Jouvet et al M 2.7 S, R, C Yes Moderate NA Yes 70 (also in Fevre- Montage et al) [1,4] 2 28 F 2.3 S, R Yes Moderate NA Yes F >3.0 S, R Yes Moderate NA Yes M 3.2 S, R, C Yes Moderate NA No F >4.0 S, R, C Yes Moderate NA Yes, Spinal 24 Dissemination 6 42 F 2.6 S, R, C Yes Moderate NA Yes 36 Fevre-Montage 7 43 M 2.0 S, R Yes NA NA Yes 18 et al. 3,4 [1,2,10] 8 14 M NA S Yes NA NA No NA 9 32 M 3.0 S, R Yes NA NA Yes M NA S, R Yes NA NA Yes M 2.5 S, R Yes NA NA No F NA S Yes NA NA Yes F 4.0 S Yes NA NA No NA F NA S, R, C Yes NA NA No F 2.5 S Yes NA NA No M 5.0 S, R Yes NA NA No F 2.0 S, R, C Yes NA NA Yes F 2.2 S, R Yes NA NA Yes F NA S, R Yes NA NA No F 1.8 S, R, C Yes NA NA Yes M NA S Yes NA NA No F 2.8 S, R, C Yes NA NA Yes M NA S, R Yes NA NA No M 2.8 S, R NA NA NA No M 5.0 S, R, C Yes Moderate NA Yes M 4.8 S, R Yes Moderate NA Yes F 3.0 S, R, C Yes Moderate NA Yes F 5.0 S Yes Moderate NA No F 3.0 S, R Yes Moderate NA Yes F 1.7 S, R Yes Moderate NA No M 4.0 S Yes Moderate NA Yes 144 Shibahara et al. [17] F 3.0 S, R, C NA Small Number 5.0% No 9 Boco et al. [7] M 2.5 S, R No Sparse 4.5% No 26 Buffenoir et al. [5] M 3.1 S, R No Rare NA No 24 (1 to10/10hpf) Kawahara et al. [13] F 2.0 S NA NA NA No 8 Fevre-Montange et al F 3.9 NA NA High 8.0% No NA [23] (13/10 HPF) Dagnew et al. [9] F 2.5 S, R NA Moderate NA No F 2.3 S, R NA Moderate NA No F 2.0 S, R NA Moderate NA NA <3 Santarius et al. [14] M 4.5 S, R No Occasional 3.0% No 84 (2/10HPF) Cerase et. al. [8] M NA S, R Yes None Observed 8.0% No 29 Sato et al. [15] M 3.2 R, C NA NA Extensive 12 dissemination Yano et al. [19] M 3.0 S, R, C No Not Observed 7.4% Yes 218 (initial) 3.3% (recurrent)
7 180 Annals of Clinical & Laboratory Science, vol. 41, no. 2, 2011 Continuation of Table 1. Review of Clinical and Histological Data from 59 reported cases of PTPR. Source Case Age Size (cm) Therapy 1 Necrosis Mitoses 2 MIB-1 Recurrence Follow-up (Years)/Sex Percentage (months) Nakamura et al. [6] M NA S, R, C NA NA 2.6% No 180 Dhillon et al. [26] F 3.0 S NA Scattered 7.8% NA 3 (4/10HPF) Varikatt et al. [18] F NA R NA NA NA Yes 121 Inoue et al. [11] M NA S, R, C NA NA 13.1% No 12 Kern et al. [12] F 2.0 S, R NA Very Sparse NA No 22 Sharma et al. [16] M NA S, R No Occasional 4.0% No F NA S, R No Occasional 3.0% No M NA S, R, C Yes Very Lively 8.0% No 15 Chang et al. [21] F NA S NA NA NA NA NA F NA S NA NA NA NA NA F NA S NA NA NA NA NA F NA S NA NA NA NA NA Hasselblatt et al. [10] M NA NA NA Moderate NA NA NA (0/10 HPF) F NA NA NA Moderate NA NA NA (0/10 HPF) Rickard et al 58 48M 2.1 S, R, C Yes <5/10 HPF 15-20% No F 1.8 S, R, C No Not Prominent % No 18 (<1/10 HPF) NA=Not available 1 The following abbreviations are used for treatment modalities: S = Surgery, R= Radiation Therapy, C= Chemotherapy. 2 The authors original evaluation of mitotic activity is listed. The criteria for their description are given where available. 3 Cases 7,8,10 and 11 as well as cases appear to be evaluated in Hasselblatt et al [10]. Case 24 appears to be further discussed in Kuchelmeister et al [2]. 4 Fevre-Montage et al. reported, In general mitotic activity was moderate (median, 1 mitosis/10 HPF; range, 0-10 mitoses/10 HPF), but 6 PTPRs displayed marked mitotic activity ( 5 mitoses/10 HPF). They did not specify the cases that had the increased mitotic activity. The Ki67 proliferation index in 14 tumors was lower than 5%; in 5 tumors it was 5% to 10%, and higher than 10% in four. growth occurring within six months after the initial presentation. After surgery, radiotherapy, and chemotherapy, the patient was free of recurrence at 14 months. In addition, the case in the literature with the second highest MIB-1 (13.1%) had surgery and radiochemotherapy, and after one year the patient was doing well without neurological deficits or tumor recurrence [11]. Overall, 36 of 59 cases reported MIB-1 labeling; however, many of these figures were general findings and were not associated with a particular case. As a result, it is difficult to draw any firm conclusions as to the role a proliferative marker has in determining the progression or recurrence of the tumor, much less determining the cut-off points for prognosis. Furthermore, although reporting mitoses and the MIB-1 labeling index is helpful, a more standard approach toward their characterization would lead to more insightful picture. Recently, Fèvre-Montange et al. explored Bcl-2 expression in a PTPR case with a high proliferation index (8%) [23]. The authors reported that Bcl-2 can be involved in neuroendocrine differentiation in some tumors as well as being a proto-oncogene. Since PTPRs express neuroendocrine markers, Bcl-2 positivity may help in determining the progression of the neoplasm as well as long-term prognosis. In their case, the tumor displayed intense expression of Bcl-2 in addition to the 8% proliferation index. This is a promising finding, which will hopefully lead to further studies [23]. New areas of interest in the diagnosis and prognosis of PTPR continue to develop as pathologists further delineate this newly described entity. Measurements of melatonin levels as well as the elucidation of the enzymes in melatonin synthesis of pineal tumors have been recently explored as possible diagnostic and treatment indicators
8 [24, 25]. As more pathologists have become familiarized with the cytological presentation of PTPR, the ability to diagnose the tumor on intraoperative smear preparations has increased. By combining observations such as smear population, architecture, background, calcification, single cells, cell morphology, location, and radiology, the addition of cytologic imprints can help improve the intraoperative diagnostic power over frozen section alone [18, 26]. After analyzing our two PTPR cases and reviewing the available literature, we suggest that PTPR, while not common, is more prevalent than previously recognized. Thanks in part to the newly recognized 2007 WHO criteria, PTPR now has a solid place on which to build an information base. Many postulate that some tumors previously classified as pineocytomas, subependymomas, or ependymomas in the pineal region were, in fact, PTPR [20]. If this is true, within a few years a more complete understanding of this tumor will be revealed. As solid grading criteria are established, treatment modalities along with therapeutic guidelines will become standardized; however, at this time prognosis for PTPR remains uncertain. References 1. Fèvre-Montange M, Hasselblatt M, Figarella-Branger D, Chauveinc L, Champier J, Saint-Pierre G, Taillandier L, Coulon A, Paulus W, Fauchon F, Jouvet A. Prognosis and histopathological features in papillary tumors of the pineal region: a retrospective multicenter study of 31 cases. J Neuropathol Exp Neurol 2006;65: Kuchelmeister K, Hügens-Penzel M, Jödicke A, Schachenmayr W. Papillary tumour of the pineal region: histodiagnostic considerations. Neuropathol Appl Neurobiol 2006;32: Roncaroli F, Scheithauer BW. Papillary tumor of the pineal region and spindle cell oncocytoma of the pituitary: new tumor entities in the 2007 WHO classification. Brain Pathol 2007;17: Jouvet A, Fauchon F, Liberski P, Saint-Pierre G, Didier-Bazes M, Heitzmann A, Delisle MB, Biassette HA, Vincent S, Mikol J, Streichenberger N, Ahboucha S, Brisson C, Belin MF, Fèvre- Montange M. Papillary tumor of the pineal region. Am J Surg Pathol 2003;27: Buffenoir K, Rigoard P, Wager M, Ferrand S, Coulon A, Blanc JL, Bataille B, Listrat A. Papillary tumor of the pineal region in a child: case report and review of the literature. Childs Nerv Syst 2008;24: Nakamura H, Makino K, Kochi M, Nakazato Y, Kuratsu J. Successful treatment of neoadjuvant therapy for papillary tumor of the pineal region. Brain Tumor Pathol 2009;26: Boco T, Aalaei S, Musacchio M, Byrne R, Cochran E. Papillary Tumor of the Pineal Region. Neuropathology 2008;28: Papillary Tumor of the Pineal Region Cerase A, Vallone IM, Di Petro G, Oliveri G, Miracco C, Venturi C. Neuroradiological follow-up of the growth of papillary tumor of the pineal region: a case report. J Neurooncol 2009; 95: Dagnew E, Langford LA, Lang FF, DeMonte F. Papillary tumors of the pineal region: case report. Neurosurgery 2007;59:E953-E Hasselblatt M, Blumcke I, Jeibmann A, Rickert CH, Jouvet A, van de Nes JA, Kuchelmeister K, Brunn A, Fèvre-Montange M, Paulus W. Immunohistochemical profile and chromosomal imbalances in papillary tumours of the pineal region. Neuropathol Appl Neurobiol 2006;32: Inoue T, Kumabe T, Kanamori M, Sonoda Y, Watanabe M, Tominaga T. Papillary tumor of the pineal region: a case report. Brain Tumor Pathol 2008;25: Kern M, Robbins P, Lee G, Watson P. Papillary tumor of the pineal region-a new pathological entity. Clin Neuropathol 2006;25: Kawahara I, Tokunaga Y, Yagi N, Iseki M, Abe K, Hayashi T. Papillary tumor of the pineal region. Neurol Med Chir (Tokyo) 2007;47: Santarius T, Joseph JA, Tsang KT, O Donovan DG, Kirollos RW. Papillary tumour of the pineal region. Br J Neurosurg 2008;22: Sato TS, Kirby PA, Buatti JM, Moritani T. Papillary tumor of the pineal region: report of a rapidly progressive tumor with possible multicentric origin. Pediatr Radiol 2009;39: Sharma MC, Jain D, Sarkar C, Suri V, Garg A, Sharma BS, Mehta VS. Papillary tumor of the pineal region - a recently described entity: a report of three cases and review of the literature. Clin Neuropathol 2009;28: Shibahara J, Todo T, Morita A, Mori H, Aoki S, Fukayama M. Papillary neuroepithelial tumor the pineal region. A case report. Acta Neuropathol 2004;108: Varikatt W, Dexter M, Mahajan H, Murali R, Ng T. Usefulness of smears in intra-operative diagnosis of newly described entities of CNS. Neuropathology 2009;29: Yano H, Ohe N, Nakayama N, Shinoda J, Iwama T. Clinicopathological features from long-term observation of a papillary tumor of the pineal region (PTPR): a case report. Brain Tumor Pathol 2009;26: Jouvet A, Nakazato Y, Scheithauer BW, Paulus W. Papillary tumour of the pineal region. In: Louis D, Ohgaki H, Wiestler O, Cavenee W eds. World Health Organization Classification of Tumours of the Central Nervous System. Geneva, Switzerland: International Agency for Research on Cancer; 2007: Chang AH, Fuller GN, Debnam JM, Karis JP, Coons SW, Ross JS, Dean BL. MR imaging of papillary tumor of the pineal region. AJNR Am J Neuroradiol 2008; Epub 2007 Oct Cottrell GT, Ferguson AV. Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 2004;117: Fèvre-Montange M, Grand S, Champier J, Hoffmann D, Pasquier B, Jouvet A. Bcl-2 expression in a papillary tumor of the pineal region. Neuropathology 2008;28: Fèvre-Montange M, Champier J, Szathmari A, Brisson C, Reboul A, Mottolese C, Fauchon F, Claustrat B, Jouvet A. Histological features and expression of enzymes implicated in melatonin synthesis in pineal parenchymal tumours and in cultured tumoural pineal cells. Neuropathol Appl Neurobiol 2008;34: Leston J, Mottolese C, Champier J, Jouvet A, Brun J, Sindou M, Chazot G, Claustrat B, Fèvre-Montange M. Contribution of the daily melatonin profile to diagnosis of tumors of the pineal region. J Neurooncol 2009;93: Dhillon J, Krishnamurthy S, Fuller GN. Papillary tumor of the pineal region: diagnosis by cytology smear. Cytopathology 2009;21; Epub 2009 Oct 13.
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