medigraphic.com
ISSN 0028-3851 (Print)

2018, Number 1

<< Back Next >>

Rev Neurol Neurocir Psiquiat 2018; 46 (1)

Molecular biomarkers involved in the World Health Organization’s new classification of gliomas

González-Aguilar A, Hernández HA, Peiro-Osuna P, Gutiérrez-Aceves A, Reyes-Moreno I

Language: Spanish
References: 99
Page: 4-13
PDF size: 314.31 Kb.


ABSTRACT

Traditionally the classification system for glial tumors of the World Health Organization (WHO) provided the basis for defining tumors with respect to their histological characteristics. The new WHO classification for the classification of brain tumors has included in its recent review, the application of molecular biology techniques as a diagnostic tool. Detection of the 1p/19q codeletion, the sequencing of the isocitrate dehydrogenase 1 (IDH1) 132 gene mutation and the immunohistochemestry determination of specific monoclonal antibodies against the R132 IDH1 protein, the TP53 and ATRX proteins, are found as the most representative techniques for the diagnosis and classification of gliomas. Already adopted worldwide, it is the result of a satisfactory consensus that meets criteria of histological, molecular and prognostic classifications, thus becoming a powerful tool that should be applied routinely in all centers.


REFERENCES

  1. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene. 2004; 23 (43): 7267-7273.

  2. Stiles CD, Rowitch DH. Glioma stem cells: a midterm exam. Neuron. 2008; 58 (6): 832-846.

  3. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114 (2): 97-109.

  4. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella- Branger D, Cavenee WK et al. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol. 2016; 131 (6): 803-820.

  5. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008; 321 (5897): 1807-1812.

  6. Sanson M, Marie Y, Paris S, Idbaih A, Laffaire J, Ducray F et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol. 2009; 27 (25): 4150-4154.

  7. Chotirat S, Thongnoppakhun W, Promsuwicha O, Boonthimat C, Auewarakul CU. Molecular alterations of isocitrate dehydrogenase 1 and 2 (IDH1 and IDH2) metabolic genes and additional genetic mutations in newly diagnosed acute myeloid leukemia patients. J Hematol Oncol. 2012; 5: 5.

  8. Borger DR, Tanabe KK, Fan KC, Lopez HU, Fantin VR, Straley KS et al. Frequent mutation of isocitrate dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping. Oncologist. 2012; 17 (1): 72-79.

  9. Hartmann C, Meyer J, Balss J, Capper D, Mueller W, Christians A et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol. 2009; 118 (4): 469-474.

  10. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 2010; 465 (7300): 966.

  11. Labussière M, Idbaih A, Wang XW, Marie Y, Boisselier B, Falet C et al. All the 1p19q codeleted gliomas are mutated on IDH1 or IDH2. Neurology. 2010; 74 (23): 1886-1890.

  12. Camelo-Piragua S, Jansen M, Ganguly A, Kim JC, Louis DN, Nutt CL. Mutant IDH1-specific immunohistochemistry distinguishes diffuse astrocytoma from astrocytosis. Acta Neuropathol. 2010; 119 (4): 509-511.

  13. Capper D, Weissert S, Balss J, Habel A, Meyer J, Jäger D et al. Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol. 2010; 20 (1): 245-254.

  14. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009; 360 (8): 765-773.

  15. Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP. Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol. 1994; 145 (5): 1175-1190.

  16. Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR et al. Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst. 1998; 90 (19): 1473-1479.

  17. Abrey LE, Louis DN, Paleologos N, Lassman AB, Raizer JJ, Mason W et al. Survey of treatment recommendations for anaplastic oligodendroglioma. Neuro Oncol. 2007; 9 (3): 314-318.

  18. Glass J, Hochberg FH, Gruber ML, Louis DN, Smith D, Rattner B. The treatment of oligodendrogliomas and mixed oligodendroglioma-astrocytomas with PCV chemotherapy. J Neurosurg. 1992; 76 (5): 741-745.

  19. Kouwenhoven MC, Kros JM, French PJ, Biemond-ter Stege EM, Graveland WJ, Taphoorn MJ et al. 1p/19q loss within oligodendroglioma is predictive for response to first line temozolomide but not to salvage treatment. Eur J Cancer. 2006; 42 (15): 2499-2503.

  20. Bauman GS, Ino Y, Ueki K, Zlatescu MC, Fisher BJ, Macdonald DR et al. Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys. 2000; 48 (3): 825-830.

  21. Jenkins RB, Blair H, Ballman KV, Giannini C, Arusell RM, Law M et al. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res. 2006; 66 (20): 9852-9861.

  22. Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM et al. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol. 2000; 18 (3): 636-645.

  23. Kouwenhoven MC, Gorlia T, Kros JM, Ibdaih A, Brandes AA, Bromberg JE et al. Molecular analysis of anaplastic oligodendroglial tumors in a prospective randomized study: A report from EORTC study 26951. Neuro Oncol. 2009; 11 (6): 737-746.

  24. Wick W, Hartmann C, Engel C, Stoffels M, Felsberg J, Stockhammer F et al. NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol. 2009; 27 (35): 5874-5880.

  25. Idbaih A, Omuro A, Ducray F, Hoang-Xuan K. Molecular genetic markers as predictors of response to chemotherapy in gliomas. Curr Opin Oncol. 2007; 19 (6): 606-611.

  26. Kaloshi G, Benouaich-Amiel A, Diakite F, Taillibert S, Lejeune J, Laigle-Donadey F et al. Temozolomide for low-grade gliomas: predictive impact of 1p/19q loss on response and outcome. Neurology. 2007; 68 (21): 1831-1836.

  27. Levin N, Lavon I, Zelikovitsh B, Fuchs D, Bokstein F, Fellig Y et al. Progressive low-grade oligodendrogliomas: response to temozolomide and correlation between genetic profile and O6-methylguanine DNA methyltransferase protein expression. Cancer. 2006; 106 (8): 1759-1765.

  28. Hoang-Xuan K, Capelle L, Kujas M, Taillibert S, Duffau H, Lejeune J et al. Temozolomide as initial treatment for adults with low-grade oligodendrogliomas or oligoastrocytomas and correlation with chromosome 1p deletions. J Clin Oncol. 2004; 22 (15): 3133-3138.

  29. Walker C, Haylock B, Husband D, Joyce KA, Fildes D, Jenkinson MD et al. Clinical use of genotype to predict chemosensitivity in oligodendroglial tumors. Neurology. 2006; 66 (11): 1661-1667.

  30. Brandes AA, Tosoni A, Cavallo G, Reni M, Franceschi E, Bonaldi L et al. Correlations between O6-methylguanine DNA methyltransferase promoter methylation status, 1p and 19q deletions, and response to temozolomide in anaplastic and recurrent oligodendroglioma: a prospective GICNO study. J Clin Oncol. 2006; 24 (29): 4746-4753.

  31. Weller M, Berger H, Hartmann C, Schramm J, Westphal M, Simon M et al. Combined 1p/19q loss in oligodendroglial tumors: predictive or prognostic biomarker? Clin Cancer Res. 2007; 13 (23): 6933-6937.

  32. Ricard D, Kaloshi G, Amiel-Benouaich A, Lejeune J, Marie Y, Mandonnet E et al. Dynamic history of low-grade gliomas before and after temozolomide treatment. Ann Neurol. 2007; 61 (5): 484-490.

  33. Kaloshi G, Guillevin R, Martin-Duverneuil N, Laigle-Donadey F, Psimaras D, Marie Y et al. Gray matter involvement predicts chemosensitivity and prognosis in gliomatosis cerebri. Neurology. 2009; 73 (6): 445-449.

  34. Ichimura K, Pearson DM, Kocialkowski S, Bäcklund LM, Chan R, Jones DT et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol. 2009; 11 (4): 341-347.

  35. Idbaih A, Marie Y, Pierron G, Brennetot C, Hoang-Xuan K, Kujas M et al. Two types of chromosome 1p losses with opposite significance in gliomas. Ann Neurol. 2005; 58 (3): 483-487.

  36. Ducray F, Idbaih A, de Reyniès A, Bièche I, Thillet J, Mokhtari K et al. Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol Cancer. 2008; 7: 41.

  37. Smith JS, Alderete B, Minn Y, Borell TJ, Perry A, Mohapatra G et al. Localization of common deletion regions on 1p and 19q in human gliomas and their association with histological subtype. Oncogene. 1999; 18 (28): 4144-4152.

  38. Griffin CA, Burger P, Morsberger L, Yonescu R, Swierczynski S, Weingart JD et al. Identification of der(1;19)(q10;p10) in five oligodendrogliomas suggests mechanism of concurrent 1p and 19q loss. J Neuropathol Exp Neurol. 2006; 65 (10): 988-994.

  39. Nutt CL. Molecular genetics of oligodendrogliomas: a model for improved clinical management in the field of neurooncology. Neurosurg Focus. 2005; 19 (5): E2.

  40. Aldape K, Burger PC, Perry A. Clinicopathologic aspects of 1p/19q loss and the diagnosis of oligodendroglioma. Arch Pathol Lab Med. 2007; 131 (2): 242-251.

  41. Eoli M, Bissola L, Bruzzone MG, Pollo B, Maccagnano C, De Simone T et al. Reclassification of oligoastrocytomas by loss of heterozygosity studies. Int J Cancer. 2006; 119 (1): 84-90.

  42. Reifenberger G, Louis DN. Oligodendroglioma: toward molecular definitions in diagnostic neuro-oncology. J Neuropathol Exp Neurol. 2003; 62 (2): 111-126.

  43. Snuderl M, Eichler AF, Ligon KL, Vu QU, Silver M, Betensky RA et al. Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res. 2009; 15 (20): 6430-6437.

  44. Tang Q, Lian Y, Yu J, Wang Y, Shi Z, Chen L. Anatomic mapping of molecular subtypes in diffuse glioma. BMC Neurol. 2017 Sep 15;17 (1): 183.

  45. Yip S, Iafrate AJ, Louis DN. Molecular diagnostic testing in malignant gliomas: a practical update on predictive markers. J Neuropathol Exp Neurol. 2008; 67 (1): 1-15.

  46. Zlatescu MC, TehraniYazdi A, Sasaki H, Megyesi JF, Betensky RA, Louis DN et al. Tumor location and growth pattern correlate with genetic signature in oligodendroglial neoplasms. Cancer Res. 2001; 61 (18): 6713-6715.

  47. Laigle-Donadey F, Martin-Duverneuil N, Lejeune J, Crinière E, Capelle L, Duffau H et al. Correlations between molecular profile and radiologic pattern in oligodendroglial tumors. Neurology. 2004; 63 (12): 2360-2362.

  48. Intergroup Radiation Therapy Oncology Group Trial 9402, Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B et al. Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol. 2006; 24 (18): 2707-2714.

  49. van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol. 2006; 24 (18): 2715-2722.

  50. Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF et al. Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget. 2012; 3 (7): 709-722.

  51. Stayton CL, Dabovic B, Gulisano M, Gecz J, Broccoli V, Giovanazzi S et al. Cloning and characterization of a new human Xq13 gene, encoding a putative helicase. Hum Mol Genet. 1994; 3 (11): 1957-1964.

  52. Picketts DJ, Higgs DR, Bachoo S, Blake DJ, Quarrell OW, Gibbons RJ. ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum Mol Genet. 1996; 5 (12): 1899-1907.

  53. Villard L, Lossi AM, Cardoso C, Proud V, Chiaroni P, Colleaux L et al. Determination of the genomic structure of the XNP/ATRX gene encoding a potential zinc finger helicase. Genomics. 1997; 43 (2): 149-155.

  54. Reuss DE, Sahm F, Schrimpf D, Wiestler B, Capper D, Koelsche C et al. ATRX and IDH1-R132H immunohistochemistry with subsequent copy number analysis and IDH sequencing as a basis for an “integrated” diagnostic approach for adult astrocytoma, oligodendroglioma and glioblastoma. Acta Neuropathol. 2015; 129 (1): 133-146.

  55. Ebrahimi A, Skardelly M, Bonzheim I, Ott I, Mühleisen H, Eckert F et al. ATRX immunostaining predicts IDH and H3F3A status in gliomas. Acta Neuropathol Commun. 2016; 4 (1): 60.

  56. Takano S, Ishikawa E, Sakamoto N, Matsuda M, Akutsu H, Noguchi M et al. Immunohistochemistry on IDH 1/2, ATRX, p53 and Ki-67 substitute molecular genetic testing and predict patient prognosis in grade III adult diffuse gliomas. Brain Tumor Pathol. 2016; 33 (2): 107-116.

  57. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R et al. Cell. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. 2006; 126 (1): 107-120.

  58. Bensaad K, Cheung EC, Vousden KH. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J. 2009; 28 (19): 3015-3026.

  59. Hasegawa H, Yamada Y, Iha H, Tsukasaki K, Nagai K, Atogami S et al. Activation of p53 by Nutlin-3a, an antagonist of MDM2, induces apoptosis and cellular senescence in adult T-cell leukemia cells. Leukemia. 2009; 23 (11): 2090-2101.

  60. Okar DA, Manzano A, Navarro-Sabatè A, Riera L, Bartrons R, Lange AJ. PFK-2/FBPase-2: maker and breaker of the essential biofactor fructose-2,6-bisphosphate. Trends Biochem Sci. 2001; 26 (1): 30-35.

  61. Obach M, Navarro-Sabaté A, Caro J, Kong X, Duran J, Gómez M et al. 6-Phosphofructo-2-kinase (pfkfb3) gene promoter contains hypoxia-inducible factor-1 binding sites necessary for transactivation in response to hypoxia. J Biol Chem. 2004; 279 (51): 53562-53570.

  62. Sathornsumetee S, Reardon DA, Desjardins A, Quinn JA, Vredenburgh JJ, Rich JN. Molecularly targeted therapy for malignant glioma. Cancer. 2007; 110 (1): 13-24.

  63. Russo AL, Kwon HC, Burgan WE, Carter D, Beam K, Weizheng X et al. Clin Cancer Res. In vitro and in vivo radiosensitization of glioblastoma cells by the poly (ADP-ribose) polymerase inhibitor E7016. 2009; 15 (2): 607-612.

  64. Dewhirst MW, Cao Y, Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer. 2008; 8 (6): 425-437.

  65. Gottlieb E, Vousden KH. p53 regulation of metabolic pathways. Cold Spring Harb Perspect Biol. 2010; 2 (4): a001040.

  66. King A, Gottlieb E. Glucose metabolism and programmed cell death: an evolutionary and mechanistic perspective. Curr Opin Cell Biol. 2009; 21 (6): 885-893.

  67. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol. 2005; 64 (6): 479-489.

  68. Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH et al. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science. 2011; 333 (6048): 1453-1455.

  69. Yip S, Butterfield YS, Morozova O, Chittaranjan S, Blough MD, An J et al. Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol. 2012; 226 (1): 7-16.

  70. Peña-Rico MA, Calvo-Vidal MN, Villalonga-Planells R, Martínez- Soler F, Giménez-Bonafé P, Navarro-Sabaté À et al. TP53 induced glycolysis and apoptosis regulator (TIGAR) knockdown results in radiosensitization of glioma cells. Radiother Oncol. 2011; 101 (1): 132-139.

  71. Silber JR, Bobola MS, Ghatan S, Blank A, Kolstoe DD, Berger MS. O6-methylguanine-DNA methyltransferase activity in adult gliomas: relation to patient and tumor characteristics. Cancer Res. 1998; 58 (5): 1068-1073.

  72. Jaeckle KA, Eyre HJ, Townsend JJ, Schulman S, Knudson HM, Belanich M et al. Correlation of tumor O6 methylguanine- DNA methyltransferase levels with survival of malignant astrocytoma patients treated with bis-chloroethylnitrosourea: a Southwest Oncology Group study. J Clin Oncol. 1998; 16 (10): 3310-3315.

  73. Martinez R, Schackert G, Yaya-Tur R, Rojas-Marcos I, Herman JG, Esteller M. Frequent hypermethylation of the DNA repair gene MGMT in long-term survivors of glioblastoma multiforme. J Neurooncol. 2007; 83 (1): 91-93.

  74. Pollack IF, Hamilton RL, Sobol RW, Burnham J, Yates AJ, Holmes EJ et al. O6-methylguanine-DNA methyltransferase expression strongly correlates with outcome in childhood malignant gliomas: results from the CCG-945 Cohort. J Clin Oncol. 2006; 24 (21): 3431-3437.

  75. Everhard S, Kaloshi G, Crinière E, Benouaich-Amiel A, Lejeune J, Marie Y et al. MGMT methylation: a marker of response to temozolomide in low-grade gliomas. Ann Neurol. 2006; 60 (6): 740-743.

  76. Gerstner ER, Yip S, Wang DL, Louis DN, Iafrate AJ, Batchelor TT. Mgmt methylation is a prognostic biomarker in elderly patients with newly diagnosed glioblastoma. Neurology. 2009; 73 (18): 1509-1510.

  77. Hau P, Stupp R, Hegi ME. MGMT methylation status: the advent of stratified therapy in glioblastoma? Dis Markers. 2007; 23 (1-2): 97-104.

  78. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med. 2000; 343 (19): 1350-1354.

  79. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005; 352 (10): 997-1003.

  80. Fraga MF, Esteller M. DNA methylation: a profile of methods and applications. Biotechniques. 2002; 33 (3): 632, 634, 636-649.

  81. Preusser M. MGMT analysis at DNA, RNA and protein levels in glioblastoma tissue. Histol Histopathol. 2009; 24 (4): 511-518.

  82. Maxwell JA, Johnson SP, Quinn JA, McLendon RE, Ali-Osman F, Friedman AH et al. Quantitative analysis of O6-alkylguanine- DNA alkyltransferase in malignant glioma. Mol Cancer Ther. 2006; 5 (10): 2531-2539.

  83. Jeuken JW, Cornelissen SJ, Vriezen M, Dekkers MM, Errami A, Sijben A et al. MS-MLPA: an attractive alternative laboratory assay for robust, reliable, and semiquantitative detection of MGMT promoter hypermethylation in gliomas. Lab Invest. 2007; 87 (10): 1055-1065.

  84. Nakasu S, Fukami T, Baba K, Matsuda M. Immunohistochemical study for O6-methylguanine-DNA methyltransferase in the nonneoplastic and neoplastic components of gliomas. J Neurooncol. 2004; 70 (3): 333-340.

  85. Preusser M, Charles Janzer R, Felsberg J, Reifenberger G, Hamou MF, Diserens AC et al. Anti-O6-methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol. 2008; 18 (4): 520-532.

  86. Weller M, Stupp R, Reifenberger G, Brandes AA, van den Bent MJ, Wick W et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol. 2010; 6 (1): 39-51.

  87. Håvik AB, Brandal P, Honne H, Dahlback HS, Scheie D, Hektoen M et al. MGMT promoter methylation in gliomas-assessment by pyrosequencing and quantitative methylation-specific PCR. J Transl Med. 2012; 10: 36.

  88. Mellai M, Monzeglio O, Piazzi A, Caldera V, Annovazzi L, Cassoni P et al. MGMT promoter hypermethylation and its associations with genetic alterations in a series of 350 brain tumors. J Neurooncol. 2012; 107 (3): 617-631.

  89. Gömöri E, Pál J, Kovács B, Dóczi T. Concurrent hypermethylation of DNMT1, MGMT and EGFR genes in progression of gliomas. Diagn Pathol. 2012; 7: 8.

  90. Hashimoto K, Narita Y, Matsushita Y, Miyakita Y, Ono M, Kayama T et al. Methylation status of O6-methylguanine-DNA-methyl transferase promoter region in non-small-cell lung cancer patients with brain metastasis. Clin Transl Oncol. 2012; 14 (1): 31-35.

  91. Silber JR, Bobola MS, Blank A, Chamberlain MC. O(6)- methylguanine-DNA methyltransferase in glioma therapy: promise and problems. Biochim Biophys Acta. 2012; 1826 (1): 71-82.

  92. Iliadis G, Kotoula V, Chatzisotiriou A, Televantou D, Eleftheraki AG, Lambaki S et al. Volumetric and MGMT parameters in glioblastoma patients: survival analysis. BMC Cancer. 2012; 12: 3.

  93. Reifenberger G, Hentschel B, Felsberg J, Schackert G, Simon M, Schnell O et al. Predictive impact of MGMT promoter methylation in glioblastoma of the elderly. Int J Cancer. 2012; 131 (6): 1342-1350.

  94. Brandes AA, Franceschi E, Tosoni A, Blatt V, Pession A, Tallini G et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol. 2008; 26 (13): 2192-2197.

  95. Fabi A, Russillo M, Metro G, Vidiri A, Di Giovanni S, Cognetti F. Pseudoprogression and MGMT status in glioblastoma patients: implications in clinical practice. Anticancer Res. 2009; 29 (7): 2607-2610.

  96. Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr Opin Neurol. 2009; 22 (6): 633-638.

  97. Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY. Effect of adding temozolomide to radiation therapy on the incidence of pseudo-progression. J Neurooncol. 2009; 94 (1): 97-101.

  98. Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PA et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. Cancer. 2008; 113 (2): 405-410.

  99. Yamasaki F, Kurisu K, Aoki T, Yamanaka M, Kajiwara Y, Watanabe Y et al. Advantages of high b-value diffusion-weighted imaging to diagnose pseudo-responses in patients with recurrent glioma after bevacizumab treatment. Eur J Radiol. 2012; 81 (10): 2805-2810.




2020     |     www.medigraphic.com