Occipital anaplastic oligodendroglioma with multiple organ metastases after a short clinical course: a case report and literature review

Diagnostic Pathology

Guodong Gao¹  Yongsheng Zhang⁴  Shiming He¹  Haixia Yang¹  Guangbin Cui⁵  Li Gong²  Hongjuan Liang¹  Tianbo Jin³  Jianghong Zhang¹  Zhiguo Zhang¹  Gang Li¹ 

[1] Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi’an 710038, P.R China;Department of Pathology, Tangdu Hospital, Fourth Military Medical University, Xi’an 710038, P.R China;National Engineering Research Center for Miniaturized Detection Systems, School of Life Sciences, Northwest University, Xi’an 710069, P.R China;Department of Administrative, Tangdu Hospital, Fourth Military Medical University, Xi'an 710038, P.R. China;Department of Radiology, Tangdu Hospital, Fourth Military Medical University, Xi’an 710038, P.R China

关键词: Genetic analysis;    Chromosome deletions;    1p/19q;    Autopsy;    Extracranial metastasis;    Oligodendroglioma;   

Others  :  867914
DOI  :  10.1186/1746-1596-9-17

 received in 2013-12-01, accepted in 2013-12-31,  发布年份 2014

【 摘 要 】

Background

It is generally believed that malignant gliomas never metastasize outside the central nervous system (CNS). However, the notion that oligodendrogliomas (OGDs) cells cannot spread outside CNS is being challenged.

Methods

We described in detail the clinical story of one patient with anaplastic OGD, which metastasized to lymph nodes, bone marrowand bones Genetic analyses included detection of 1p and 19q chromosomal arms, methylation status of MGMT promoter, and PTEN exon mutations. A search of worldwide literature was conducted for reports of metastatic OGDs using NCBI-PubMed, with the keywords “extracranial”, “extraneural”, “oligodendroglioma”, “oligodendrogliomas”, “metastatic”, “metastasis”, and “metastases”, in different combinations.

Results

An open biopsy of the infiltrated bones in our patient revealed that malignant cells had replaced the patient’s marrow. Moreover, the diagnosis of multiple-organ metastases of anaplastic OGD was confirmed based on immunohistochemical staining. Genetic analyses showed that the tumors originated from previously resected brain lesions. None of the lesions had 1p and 19q deletions, but hypermethylation of MGMT promoter, and the G → A transversion at codon 234 of PTEN exon 2 were detected. Literatures review yielded 60 reports of metastatic OGDs from 1951 to the present, which with our patient makes 61 cases. Concerning these 61 patients, there were 110 infiltrated sites correlated closely with primary OGDs. The most frequent metastatic sites were bone and bone marrow (n = 47; 42.7%), lymph nodes (n = 22; 20.0%), liver (n = 7; 6.4%), scalp (n = 6; 5.5%), lung (n = 6; 5.5%), pleura (n = 4; 3.6%), chest wall (n = 3; 2.7%), iliopsoas muscle (n = 2; 1.8%), soft tissue (n = 2; 1.8%), and parotid gland (n = 2; 1.8%).

Conclusions

Extracranial metastases in anaplastic OGD are very rare but they do occur; bone and bone marrow may be the most common sites. Detection of certain molecular markers such as deletion of 1p and 19q chromosomal arms, hypermethylation of MGMT promoter, and characteristic PTEN exon mutations may help differentiate subtypes which are more prone to extracranial metastases.

Virtual slides

The virtual slide(s) for this article can be found here: http://www.diagnosticpathology.diagnomx.eu/vs/8749838611478560 webcite.

【 授权许可】

   
2014 Li et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Bailey P, Cushing P: A Classification of the Tumors of the Glioma Group on Histogenetic Basis with Correlated Study of Prognosis. Philadelphia: J.B. Lippincott; 1926:175.
• [2]Smith DR, Hardman JM, Earle KM: Metastasizing neuroectodermal tumors of the central nervous system. J Neurosurg 1969, 31:50-58.
• [3]Liwnicz BH, Rubinstein LJ: The pathways of extraneural spread in metastasizing gliomas: a report of three cases and critical review of the literature. Hum Pathol 1979, 10:453-467.
• [4]Han SR, Yoon SW, Yee GT, Choi CY, Lee DJ, Sohn MJ, Chang SH, Whang CJ: Extraneural metastases of anaplastic oligodendroglioma. J Clin Neurosci 2008, 15:946-949.
• [5]McLendon RE, Bentley RC, Parisi JE, Tien RD, Harrison JC, Tarbell NJ, Billitt AL, Gualtieri RJ, Friedman HS: Malignant supratentorial glial-neuronal neoplasms: report of two cases and review of the literature. Arch Pathol Lab Med 1997, 121:485-492.
• [6]Tatar Z, Thivat E, Planchat E, Gimbergues P, Gadea E, Abrial C, Durando X: Temozolomide and unusual indications: review of literature. Cancer Treat Rev 2013, 39:125-135.
• [7]Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P: The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007, 114:97-109.
• [8]Giannini C, Scheithauer BW, Weaver AL, Burger PC, Kros JM, Mork S, Graeber MB, Bauserman S, Buckner JC, Burton J, Riepe R, Tazelaar HD, Nascimento AG, Crotty T, Keeney GL, Pemicone P, Altermatt H: Oligodendrogliomas: reproducibility and prognostic value of histologic diagnosis and grading. J Neuropathol Exp Neurol 2001, 60:248-282.
• [9]Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO: European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group: effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009, 10:459-466.
• [10]Hegi ME, Liu L, Herman JG, Stupp R, Wick W, Weller M, Mehta MP, Gilbert MR: Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol 2008, 26:4189-4199.
• [11]Reineke T, Jenni B, Abdou MT, Frigerio S, Zubler P, Moch H, Tinguely M: Ultrasonic decalcification offers new perspectives for rapid FISH, DNA, and RT-PCR analysis in bone marrow trephines. Am J Surg Pathol 2006, 30:892-896.
• [12]Mehdi SJ, Alam MS, Batra S, Rizvi MMA: Allelic loss at 6q25–27, the Parkin tumor suppressor gene locus in cervical carcinoma. Med Oncol 2011, 28:1520-1526.
• [13]Sambrook J, Russell DW: Molecular cloning: A laboratory manual. 3rd edition. Cold Spring Harbor Lab. Press: Cold Spring Harbor; 2001.
• [14]Dong Z, Pang JS, Ng MH, Poon WS, Zhou L, Ng HK: Identification of two contiguous minimally deleted regions on chromosome 1p36.31-p36.32 in oligodendroglial tumors. Br J Cancer 2004, 91:1105-1111.
• [15]Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005, 352:997-1003.
• [16]Eng C: PTEN: one gene, many syndromes. Hum Mutat 2003, 22:183-198.
• [17]Zheng H, Takahashi H, Murai Y, Cui Z, Nomoto K, Tsuneyama K, Takano Y: Low expression of FHIT and PTEN correlates with malignancy of gastric carcinomas: tissue-array findings. Appl Immunohistochem Mol Morphol 2007, 15:432-440.
• [18]Ali A, Saluja SS, Hajela K, Mishra PK, Rizvi MA: Mutational and expressional analyses of PTEN gene in colorectal cancer from Northern India. Mol Carcinog 2013. 10.1002/mc.22001. [Epub ahead of print]
• [19]Rizvi MA, Shabbir MA, Ali A, Mehdi SJ, Batra S, Mandal AK: Aberrant promoter methylation and inactivation of PTEN gene in cervical carcinoma from Indian population. J Cancer Res Clin Oncol 2011, 137:1255-1262.
• [20]Guo CY, Xu XF, Wu JY, Liu SF: PCR–SSCP-DNA sequencing method in detecting PTEN gene mutation and its significance in human gastric cancer. World J Gastroenterol 2008, 14:3804-3811.
• [21]Garner J, Morcos Y, Bari M: Extradural cord compression due to metastatic oligodendroglioma. J Neurooncol 2002, 58:71-75.
• [22]Subramanian A, Harris A, Piggott K, Shieff C, Bradford R: Metastasis to and from the central nervous system: the ‘relatively protected site’. Lancet Oncol 2002, 3:498-507.
• [23]Al-Ali F, Hendon AJ, Liepman MK, Wisniewski JL, Krinock MJ, Beckman K: Oligodendroglioma metastatic to bone marrow. AJNR Am J Neuroradiol 2005, 26:2410-2414.
• [24]Fayeye O, Sankaran V, Sherlala K, Choksey M: Oligodendroglioma presenting with intradural spinal metastases: an unusual cause of cauda equine syndrome. J Clin Neurosci 2010, 17:265-267.
• [25]Shaw EG, Scheithauer BW, O’Fallon JR, Tazelaar HD, Davis DH: Oligodendrogliomas: the Mayo Clinic experience. J Neurosurg 1992, 76:428-434.
• [26]James TGI, Pagel W: Oligodenroglioma with extracranial metastases. Br J Surg 1951, 39:56-65.
• [27]Spataro J, Sacks O: Oligodendroglioma with remote metastases. Case report. J Neurosurg 1968, 28:373-379.
• [28]Jellinger K, Minauf M, Salzer-Kuntschik M: Oligodendroglioma with extraneural metastases. J Neurol Neurosurg Psychiatry 1969, 32:249-253.
• [29]Schuster H, Jellinger K, Gund A, Regele H: Extracranial metastases of anaplastic cerebral gliomas. Acta Neurochir (Wien) 1976, 35:247-259.
• [30]Kernohan JW: Oligodendrogliomas. In Minckler J (ed) Pathology of the nervous system. Vol 2 edition. New York: McGraw-Hill Co; 1971. 1993–2007
• [31]Eade OE, Urich H: Metastasising gliomas in young subjects. J Pathol 1971, 103:245-256.
• [32]Cappalaere P, Clay A, Adenis L, Demaille A, Laine E: Les metastases des tumors cerebrales primitives en dehors du nevraxe: a propos de trios observations. Bull Cancer (Paris) 1972, 59:235-254.
• [33]Brander WL, Turner DR: Extracranial metastases from a glioma in the absence of surgical intervention. J Neurol Neurosurg Psychiatry 1975, 38:1133-1135.
• [34]Kummer RV, Volk B, Dorndorf W: Extraneural metastasierendes oligodendrogliom. Arch Psychiatr Nervenkr 1969, 223:287-293.
• [35]Chin HW, Hazel JJ, Kim TH, Webster JH: Oligodendrogliomas. I. A clinical study of cerebral oligodendrogliomas. Cancer 1980, 45:1458-1466.
• [36]Ordonez NG, Ayala AA, Leavens ME: Extracranial metastases of oligodenroglioma: report of a case and review of the literature. Neurosurgery 1981, 8:391-395. comments 395–396
• [37]Nakamura O, Watanabe T, Nomura K, Nakajima T: Diffuse bone marrow metastasis of an anaplastic oligodendroglioma. No Shinkei Geka 1985, 13:903-909.
• [38]Newman HFV, Howard GCV, Reid PM: Metastatic oligodendroglioma presenting as a leukoerythroblastic anaemia. Eur J Surg Onc 1985, 11:287-288.
• [39]Macdonald DR, O’Brien RA, Gilbert JJ, Cairncross JG: Metastatic anaplastic oligodendroglioma. Neurology 1989, 39:1593-1596.
• [40]Rolski J, Rzepecki W, Kałuza J, Zemełka T, Zuchowska-Vogelgesang B: A rare case of dissemination of anaplastic oligodendroma outside the central nervous system. Neurol Neurochir Pol 1993, 27:93-97.
• [41]Steininger H, von Streitberg U: Oligodendroglioma with cervical lymph node metastasis. Pathologe 1993, 14:386-390.
• [42]Gerrard GE, Bond MG, Jack AS: Bone marrow infiltration by a parietal lobe grade III oligodendroglioma. Clin Oncol (R Coll Radiol) 1995, 7:321-322.
• [43]Schröder R, Lorenzen J, Ostertag H, Ortmann M, Hansmann ML: Extraneural metastasis of brain and spinal cord tumors. Report of 2 cases. Pathologe 1995, 16:223-229.
• [44]Monzani V, Rovellini A, Masini B, Cappricci E, Miserocchi G: Metastatic oligodendroglioma. Case report. J Neurol Sci 1996, 40:239-241.
• [45]Dawson TP: Case report. Pancytopenia from a disseminated anaplastic oligodendroglioma. Neuropathol App Neurobiol 1997, 23:516-520.
• [46]Finsterer J, Breiteneder S, Mueller MR, Wogritsch C, Vesely M, Kleinert R, Pendl G, Mamoli B: Pleural and bone marrow metastasis from supratentorial oligoastrocytoma grade III. Oncology 1998, 55:345-348.
• [47]Anand M, Kumar R, Jain P, Gupta R, Ghosal N, Sharma A, Agarwal A, Sharma MC: Metastatic anaplastic oligodendroglioma simulating acute leukaemia. Acta Cytol 2003, 47:467-469.
• [48]Giordana MT, Gasverde S, Balteri I: Bone metastasis of oligodendrogliomas: clinical and molecular genetic study. Neuro Oncol 2002, 4:38e.
• [49]Sharma A, Agarwal A, Sharma MC, Anand M, Agarwal S, Raina V: Bone marrow metastasis in anaplastic oligodendroglioma. Int J Clin Pract 2003, 57:351-352.
• [50]Choon A, Roepke JE: Importance of immunohistochemichal staining in metastatic anaplastic oligodendroglioma. Arch Pathol Lab Med 2004, 128:489-490.
• [51]Morrison T, Bilbao JM, Yang G, Perry JR: Bony metastases of anaplastic oligodendroglioma respond to temozolomide. Can J Neurol Sci 2004, 31:102-108.
• [52]Wang M, Murphy KM, Kulesza P, Hatanpaa KJ, Olivi A, Tufaro A, Erozan Y, Westra WH, Burger PC, Berg KD: Molecular diagnosis of metastasizing oligodendroglioma: a case report. J Mol Diagn 2004, 6:52-57.
• [53]Merrell R, Nabors LB, Perry A, Palmer CA: 1p/19q chromosome deletions in metastatic oligodendroglioma. J Neurooncol 2006, 80:203-207.
• [54]Lee CC, Jiang JS, Chen ET, Yokoo H, Pan YH, Tsai MD: Cytologic diagnosis of a metastatic oligodendroglioma in a pleural effusion. A case report. Acta Cytol 2006, 50:542-544.
• [55]Bruggers C, White K, Zhou H, Chen Z: Extracranial relapse of an anaplastic oligodendroglioma in an adolescent: case report and review of the literature. J Pediatr Hematol Oncol 2007, 29:319-322.
• [56]Uzuka T, Kakita A, Inenaga C, Takahashi H, Tanaka R, Takahashi H: Frontal anaplastic oligodendroglioma showing multi-organ metastases after a long clinical course. Case report. Neurol Med Chir (Tokyo) 2007, 47:174-177.
• [57]Zustovich F, Della Puppa A, Scienza R, Anselmi P, Furlan C, Cartei G: Metastatic oligodendrogliomas: a review of the literature and case report. Acta Neurochir (Wien) 2008, 150:699-702. discussion 702–703
• [58]Volavsek M, Lamovec J, Popović M: Extraneural metastases of anaplastic oligodendroglial tumors. Pathol Res Pract 2009, 205:502-507.
• [59]Noshita N, Mashiyama S, Fukawa O, Asano S, Watanabe M, Tominaga T: Extracranial metastasis of anaplastic oligodendroglioma with 1p19q loss of heterozygosity–case report. Neurol Med Chir (Tokyo) 2010, 50:161-164.
• [60]Oshiro S, Komatsu F, Tsugu H, Nabeshima K, Abe H, Ohkawa M, Inoue T: A case of intramedullary cervical metastasis from cerebellar anaplastic oligodendroglioma without typical MR appearance for CSF dissemination. No Shinkei Geka 2010, 38:279-285.
• [61]Krijnen JL, Fleischeur RE, van Berkel M, Westenend PJ: Metastatic oligodendroglioma: a case report and incidence in The Netherlands. Clin Neuropathol 2010, 29:141-146.
• [62]Kural C, Pusat S, Sentürk T, Seçer Hİ, Izci Y: Extracranial metastases of anaplastic oligodendroglioma. J Clin Neurosci 2011, 18:136-138.
• [63]Wu Y, Liu B, Qu L, Tao H: Extracranial skeletal metastasis in anaplastic oligodendroglioma: case report and review of the literature. J Int Med Res 2011, 39:960-967.
• [64]Cordiano V, Miserocchi F, Storti M: Bone marrow metastases from anaplastic oligodendroglioma presenting with pancytopenia and hypogammaglobulinemia: a case report. Tumori 2011, 97:808-811.
• [65]Can B, Akpolat I, Meydan D, Üner A, Kandemir B, Söylemezoğlu F: Fine-needle aspiration cytology of metastatic oligodendroglioma: case report and literature review. Acta Cytol 2012, 56:97-103.
• [66]Alacacioglu A, Unal S, Canpolat S, Yurt A, Oztekin O, Coskun A, Karatas A, Postaci H, Sop G: Breast metastasis of anaplastic oligodendroglioma: a case report. Tumori 2012, 98:162e-164e.
• [67]Greene J, Cadoo K, Ti J, O’Donnell N, Allcutt D, Farrell M, Grogan L: 1p19q co-deleted oligodendroglioma metastatic to bone. Clin Neuropathol 2013, 32:139-141.
• [68]Gyepes MT, D’ angio GJ: Extracranial metastases from central nervous system tumors in children and adolescents. Radiology 1966, 87:55-63.
• [69]Carlsen JG, Tietze A, Lassen YA, Rosendal F: Paraplegia due to drop metastases from anaplastic oligodendroglioma. Br J Neurosurg 2012, 26:94-95.
• [70]Schweitzer T, Vince GH, Herbold C, Roosen K, Tonn JC: Extraneural metastases of primary brain tumors. J Neurooncol 2001, 53:107-114.
• [71]Hoffman HJ, Duffner PK: Extraneural metastases of central nervous system tumors. Cancer 1985, 56:1778-1782.
• [72]Mechtler LL, Nandigam K: Spinal cord tumors: new views and future directions. Neurol Clin 2013, 31:241-268.
• [73]NCCN Clinical Practice Guidelines in Oncology: Central Nervous System Cancers. Version1. 2013. http://www.nccn.org/professionals/physician_ gls/pdf/cns.pdf webcite
• [74]Cairncross JG, Ueki K, Zlatescu C, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, Ramsay DA, Louis DN: Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendroglioma. J Natl Cancer Inst 1998, 90:1473-1479.
• [75]Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB: Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 2000, 18:636-645.
• [76]Davis FG, McCarthy BJ, Freels S, Kupelian V, Bondy ML: The conditional probability of survival of patients with primary malignant brain tumors: surveillance, epidemiology, and end results (SEER) data. Cancer 1999, 85:485-491.
• [77]Scott CB, Scarantino C, Urtasun R, Movsas B, Jones CU, Simpson JR, Fischbach AJ, Curran WJ Jr: Validation and predictive power of Radiation Therapy Oncology Group (RTOG) recursive partitioning analysis classes for malignant glioma patients: a report using RTOG 90–06. Int J Radiat Oncol Biol Phys 1998, 40:51-55.
• [78]Broderick DK, Di C, Parrett TJ, Samuels YR, Cummins JM, McLendon RE, Fults DW, Velculescu VE, Bigner DD, Yan H: Mutations of PIK3CA in anaplastic oligodendrogliomas, high-grade astrocytomas, and medulloblastomas. Cancer Res 2004, 64:5048-5050.
• [79]Ino Y, Betensky RA, Zlatescu MC, Sasaki H, Macdonald DR, Stemmer-Rachamimov AO, Ramsay DA, Cairncross JG, Louis DN: Molecular subtypes of anaplastic oligodendroglioma: implications for patient management at diagnosis. Clin Cancer Res 2001, 7:839-845.
• [80]Yang Y, Shao N, Luo G, Li L, Zheng L, Nilsson-Ehle PXN: Mutations of PTEN gene in gliomas correlate to tumor differentiation and short-term survival rate. Anticancer Res 2010, 30:981-985.
• [81]Wang JY, Huang TJ, Chen FM, Hsieh MC, Lin SR, Hou MF, Hsieh JS: Mutation analysis of the putative tumor suppressor gene PTEN/MMAC1 in advanced gastric carcinomas. Virchows Arch 2003, 442:437-443.
• [82]Tate G, Suzuki T, Mitsuya T: Mutation of the PTEN gene in a human hepatic angiosarcoma. Cancer Genet Cytogenet 2007, 178:160-162.
• [83]Rizvi MM, Ali A, Mehdi SJ, Saluja SS, Mishra PK: Association of epigenetic alteration in PTEN gene with colorectal cancer progression among Indian population. Int J Colorectal Dis 2013, 28:283-284.
• [84]van den Bent MJ, Taphoorn MJ, Brandes AA, Menten J, Stupp R, Frenay M, Chinot O, Kros JM, van der Rijt CC, Vecht CJ, Allgeier A, Gorlia T: European Organization for Research and Treatment of Cancer Brain Tumor Group: Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumors: the European Organization for Research and Treatment of Cancer Brain Tumor Group Study 26971. J Clin Oncol 2003, 21:2525-2528.
• [85]Hoang-Xuan K, Capelle L, Kujas M, Taillibert S, Duffau H, Lejeune J, Polivka M, Crinière E, Marie Y, Mokhtari K, Carpentier AF, Laigle F, Simon JM, Cornu P, Broët P, Sanson M, Delattre JY: Temozolomide as initial treatment for adults with low-grade oligodendrogliomas or oligoastrocytomas and correlation with chromosome 1p deletions. J Clin Oncol 2004, 22:3133-3138.
• [86]Levin N, Lavon I, Zelikovitsh B, Fuchs D, Bokstein F, Fellig Y, Siegal T: Progressive low-grade oligodendrogliomas: response to temozolomide and correlation between genetic profile and O6- methylguanine DNA methyltransferase protein expression. Cancer 2006, 106:1759-1765.
• [87]Ziegler DS, Kung AL, Kieran MW: Antiapoptosis mechanisms in malignant gliomas. J Clin Oncol 2008, 26:493-500.
• [88]Kesari S, Schiff D, Drappatz J, LaFrankie D, Doherty L, Macklin EA, Muzikansky A, Santagata S, Ligon KL, Norden AD, Ciampa A, Bradshaw J, Levy B, Radakovic G, Ramakrishna N, Black PM, Wen PY: Phase II study of protracted daily temozolomide for lowgrade gliomas in adults. Clin Cancer Res 2009, 15:330-337.