Skip to main content
Top
Published in: Journal of Neuro-Oncology 2/2017

01-04-2017 | Clinical Study

Decreased survival in glioblastomas is specific to contact with the ventricular-subventricular zone, not subgranular zone or corpus callosum

Authors: Akshitkumar M. Mistry, Michael C. Dewan, Gabrielle A. White-Dzuro, Philip R. Brinson, Kyle D. Weaver, Reid C. Thompson, Rebecca A. Ihrie, Lola B. Chambless

Published in: Journal of Neuro-Oncology | Issue 2/2017

Login to get access

Abstract

The clinical effect of radiographic contact of glioblastoma (GBM) with neurogenic zones (NZ)—the ventricular-subventricular (VSVZ) and subgranular (SGZ) zones—and the corpus callosum (CC) remains unclear and, in the case of the SGZ, unexplored. We investigated (1) if GBM contact with a NZ correlates with decreased survival; (2) if so, whether this effect is associated with a specific NZ; and (3) if radiographic contact with or invasion of the CC by GBM is associated with decreased survival. We retrospectively identified 207 adult patients who underwent cytoreductive surgery for GBM followed by chemotherapy and/or radiation. Age, preoperative Karnofsky performance status score (KPS), and extent of resection were recorded. Preoperative MRIs were blindly analyzed to calculate tumor volume and assess its contact with VSVZ, SGZ, CC, and cortex. Overall (OS) and progression free (PFS) survivals were calculated and analyzed with multivariate Cox analyses. Among the 207 patients, 111 had GBM contacting VSVZ (VSVZ+GBMs), 23 had SGZ+GBMs, 52 had CC+GBMs, and 164 had cortex+GBMs. VSVZ+, SGZ+, and CC+ GBMs were significantly larger in size relative to their respective non-contacting controls. Multivariate Cox survival analyses revealed GBM contact with the VSVZ, but not SGZ, CC, or cortex, as an independent predictor of lower OS, PFS, and early recurrence. We hypothesize that the VSVZ niche has unique properties that contribute to GBM pathobiology in adults.
Appendix
Available only for authorised users
Literature
1.
go back to reference Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744. doi:10.1038/nature02301 CrossRefPubMed Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744. doi:10.​1038/​nature02301 CrossRefPubMed
2.
go back to reference Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386. doi:10.1038/nature10487 CrossRefPubMedPubMedCentral Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386. doi:10.​1038/​nature10487 CrossRefPubMedPubMedCentral
3.
go back to reference Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317. doi:10.1038/3305 CrossRefPubMed Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317. doi:10.​1038/​3305 CrossRefPubMed
5.
go back to reference Kroonen J, Nassen J, Boulanger YG, Provenzano F, Capraro V, Bours V, Martin D, Deprez M, Robe P, Rogister B (2011) Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int J Cancer 129:574–585. doi:10.1002/ijc.25709 CrossRefPubMed Kroonen J, Nassen J, Boulanger YG, Provenzano F, Capraro V, Bours V, Martin D, Deprez M, Robe P, Rogister B (2011) Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int J Cancer 129:574–585. doi:10.​1002/​ijc.​25709 CrossRefPubMed
6.
go back to reference Sadahiro H, Yoshikawa K, Ideguchi M, Kajiwara K, Ishii A, Ikeda E, Owada Y, Yasumoto Y, Suzuki M (2014) Pathological features of highly invasive glioma stem cells in a mouse xenograft model. Brain Tumor Pathol 31:77–84. doi:10.1007/s10014-013-0149-x CrossRefPubMed Sadahiro H, Yoshikawa K, Ideguchi M, Kajiwara K, Ishii A, Ikeda E, Owada Y, Yasumoto Y, Suzuki M (2014) Pathological features of highly invasive glioma stem cells in a mouse xenograft model. Brain Tumor Pathol 31:77–84. doi:10.​1007/​s10014-013-0149-x CrossRefPubMed
7.
go back to reference Goffart N, Kroonen J, Di Valentin E, Dedobbeleer M, Denne A, Martinive P, Rogister B (2015) Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neuro-oncol 17:81–94. doi:10.1093/neuonc/nou144 CrossRefPubMed Goffart N, Kroonen J, Di Valentin E, Dedobbeleer M, Denne A, Martinive P, Rogister B (2015) Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neuro-oncol 17:81–94. doi:10.​1093/​neuonc/​nou144 CrossRefPubMed
9.
go back to reference Chaichana KL, Jusue-Torres I, Lemos AM, Gokaslan A, Cabrera-Aldana EE, Ashary A, Olivi A, Quinones-Hinojosa A (2014) The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors? J Neurooncol 120:625–634. doi:10.1007/s11060-014-1597-9 CrossRefPubMedPubMedCentral Chaichana KL, Jusue-Torres I, Lemos AM, Gokaslan A, Cabrera-Aldana EE, Ashary A, Olivi A, Quinones-Hinojosa A (2014) The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors? J Neurooncol 120:625–634. doi:10.​1007/​s11060-014-1597-9 CrossRefPubMedPubMedCentral
10.
go back to reference Allahdini F, Amirjamshidi A, Reza-Zarei M, Abdollahi M (2010) Evaluating the prognostic factors effective on the outcome of patients with glioblastoma multiformis: does maximal resection of the tumor lengthen the median survival? World neurosurgery 73: 128–134. doi:10.1016/j.wneu.2009.06.001 (Discussion e116)CrossRefPubMed Allahdini F, Amirjamshidi A, Reza-Zarei M, Abdollahi M (2010) Evaluating the prognostic factors effective on the outcome of patients with glioblastoma multiformis: does maximal resection of the tumor lengthen the median survival? World neurosurgery 73: 128–134. doi:10.​1016/​j.​wneu.​2009.​06.​001 (Discussion e116)CrossRefPubMed
11.
go back to reference Ramakrishna R, Barber J, Kennedy G, Rizvi A, Goodkin R, Winn RH, Ojemann GA, Berger MS, Spence AM, Rostomily RC (2010) Imaging features of invasion and preoperative and postoperative tumor burden in previously untreated glioblastoma: correlation with survival. Surg Neurol Int. doi:10.4103/2152-7806.68337 CrossRefPubMedPubMedCentral Ramakrishna R, Barber J, Kennedy G, Rizvi A, Goodkin R, Winn RH, Ojemann GA, Berger MS, Spence AM, Rostomily RC (2010) Imaging features of invasion and preoperative and postoperative tumor burden in previously untreated glioblastoma: correlation with survival. Surg Neurol Int. doi:10.​4103/​2152-7806.​68337 CrossRefPubMedPubMedCentral
13.
go back to reference Chaichana K, Parker S, Olivi A, Quinones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112:997–1004. doi:10.3171/2009.9.JNS09805 CrossRefPubMed Chaichana K, Parker S, Olivi A, Quinones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112:997–1004. doi:10.​3171/​2009.​9.​JNS09805 CrossRefPubMed
14.
15.
go back to reference Tejada-Solis S, Aldave-Orzaiz G, Pay-Valverde E, Marigil-Sanchez M, Idoate-Gastearena MA, Diez-Valle R (2012) Prognostic value of ventricular wall fluorescence during 5-aminolevulinic-guided surgery for glioblastoma. Acta neurochirurgica 154: 1997–2002. doi:10.1007/s00701-012-1475-1 (Discussion 2002)CrossRefPubMed Tejada-Solis S, Aldave-Orzaiz G, Pay-Valverde E, Marigil-Sanchez M, Idoate-Gastearena MA, Diez-Valle R (2012) Prognostic value of ventricular wall fluorescence during 5-aminolevulinic-guided surgery for glioblastoma. Acta neurochirurgica 154: 1997–2002. doi:10.​1007/​s00701-012-1475-1 (Discussion 2002)CrossRefPubMed
16.
go back to reference Chaichana KL, Pendleton C, Chambless L, Camara-Quintana J, Nathan JK, Hassam-Malani L, Li G, Harsh GR, Thompson RC, Lim M, Quinones-Hinojosa A (2013) Multi-institutional validation of a preoperative scoring system which predicts survival for patients with glioblastoma. J Clin Neurosci 20:1422–1426. doi:10.1016/j.jocn.2013.02.007 CrossRefPubMedPubMedCentral Chaichana KL, Pendleton C, Chambless L, Camara-Quintana J, Nathan JK, Hassam-Malani L, Li G, Harsh GR, Thompson RC, Lim M, Quinones-Hinojosa A (2013) Multi-institutional validation of a preoperative scoring system which predicts survival for patients with glioblastoma. J Clin Neurosci 20:1422–1426. doi:10.​1016/​j.​jocn.​2013.​02.​007 CrossRefPubMedPubMedCentral
18.
go back to reference Liang TH, Kuo SH, Wang CW, Chen WY, Hsu CY, Lai SF, Tseng HM, You SL, Chen CM, Tseng WI (2015) Adverse prognosis and distinct progression patterns after concurrent chemoradiotherapy for glioblastoma with synchronous subventricular zone and corpus callosum invasion. Radiother Oncol. doi:10.1016/j.radonc.2015.11.017 CrossRefPubMed Liang TH, Kuo SH, Wang CW, Chen WY, Hsu CY, Lai SF, Tseng HM, You SL, Chen CM, Tseng WI (2015) Adverse prognosis and distinct progression patterns after concurrent chemoradiotherapy for glioblastoma with synchronous subventricular zone and corpus callosum invasion. Radiother Oncol. doi:10.​1016/​j.​radonc.​2015.​11.​017 CrossRefPubMed
20.
go back to reference Kappadakunnel M, Eskin A, Dong J, Nelson SF, Mischel PS, Liau LM, Ngheimphu P, Lai A, Cloughesy TF, Goldin J, Pope WB (2010) Stem cell associated gene expression in glioblastoma multiforme: relationship to survival and the subventricular zone. J Neurooncol 96:359–367. doi:10.1007/s11060-009-9983-4 CrossRefPubMed Kappadakunnel M, Eskin A, Dong J, Nelson SF, Mischel PS, Liau LM, Ngheimphu P, Lai A, Cloughesy TF, Goldin J, Pope WB (2010) Stem cell associated gene expression in glioblastoma multiforme: relationship to survival and the subventricular zone. J Neurooncol 96:359–367. doi:10.​1007/​s11060-009-9983-4 CrossRefPubMed
22.
23.
go back to reference Pina Batista KM, Vega IF, de Eulate-Beramendi SA, Morales J, Kurbanov A, Asnel D, Meilan A, Astudillo A (2015) Prognostic significance of the markers IDH1 and YKL40 related to the subventricular zone. Folia neuropathologica 53: 52–59.CrossRef Pina Batista KM, Vega IF, de Eulate-Beramendi SA, Morales J, Kurbanov A, Asnel D, Meilan A, Astudillo A (2015) Prognostic significance of the markers IDH1 and YKL40 related to the subventricular zone. Folia neuropathologica 53: 52–59.CrossRef
25.
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B 57: 289–300. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B 57: 289–300.
27.
go back to reference Gorlia T, van den Bent MJ, Hegi ME, Mirimanoff RO, Weller M, Cairncross JG, Eisenhauer E, Belanger K, Brandes AA, Allgeier A, Lacombe D, Stupp R (2008) Nomograms for predicting survival of patients with newly diagnosed glioblastoma: prognostic factor analysis of EORTC and NCIC trial 26981–22981/CE.3. The Lancet Oncol 9:29–38. doi:10.1016/s1470-2045(07)70384-4 CrossRefPubMed Gorlia T, van den Bent MJ, Hegi ME, Mirimanoff RO, Weller M, Cairncross JG, Eisenhauer E, Belanger K, Brandes AA, Allgeier A, Lacombe D, Stupp R (2008) Nomograms for predicting survival of patients with newly diagnosed glioblastoma: prognostic factor analysis of EORTC and NCIC trial 26981–22981/CE.3. The Lancet Oncol 9:29–38. doi:10.​1016/​s1470-2045(07)70384-4 CrossRefPubMed
29.
30.
go back to reference Curtis MA, Low VF, Faull RL (2012) Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Develop Neurobiol 72:990–1005. doi:10.1002/dneu.22028 CrossRef Curtis MA, Low VF, Faull RL (2012) Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Develop Neurobiol 72:990–1005. doi:10.​1002/​dneu.​22028 CrossRef
32.
go back to reference Iacoangeli M, Di Rienzo A, Colasanti R, Zizzi A, Gladi M, Alvaro L, Nocchi N, Di Somma LG, Scarpelli M, Scerrati M (2012) Endoscopy-verified occult subependymal dissemination of glioblastoma and brain metastasis undetected by MRI: prognostic significance. OncoTargets Ther 5: 449–456. doi:10.2147/OTT.S39429 CrossRef Iacoangeli M, Di Rienzo A, Colasanti R, Zizzi A, Gladi M, Alvaro L, Nocchi N, Di Somma LG, Scarpelli M, Scerrati M (2012) Endoscopy-verified occult subependymal dissemination of glioblastoma and brain metastasis undetected by MRI: prognostic significance. OncoTargets Ther 5: 449–456. doi:10.​2147/​OTT.​S39429 CrossRef
33.
go back to reference Hayashi Y, Nakada M, Tanaka S, Uchiyama N, Hayashi Y, Kita D, Hamada J (2010) Implication of 5-aminolevulinic acid fluorescence of the ventricular wall for postoperative communicating hydrocephalus associated with cerebrospinal fluid dissemination in patients with glioblastoma multiforme: a report of 7 cases. J Neurosurg 112:1015–1019. doi:10.3171/2009.8.JNS09516 CrossRefPubMed Hayashi Y, Nakada M, Tanaka S, Uchiyama N, Hayashi Y, Kita D, Hamada J (2010) Implication of 5-aminolevulinic acid fluorescence of the ventricular wall for postoperative communicating hydrocephalus associated with cerebrospinal fluid dissemination in patients with glioblastoma multiforme: a report of 7 cases. J Neurosurg 112:1015–1019. doi:10.​3171/​2009.​8.​JNS09516 CrossRefPubMed
36.
go back to reference Sonoda Y, Saito R, Kanamori M, Kumabe T, Uenohara H, Tominaga T (2014) The association of subventricular zone involvement at recurrence with survival after repeat surgery in patients with recurrent glioblastoma. Neurologia medico-chirurgica 54: 302–309.CrossRef Sonoda Y, Saito R, Kanamori M, Kumabe T, Uenohara H, Tominaga T (2014) The association of subventricular zone involvement at recurrence with survival after repeat surgery in patients with recurrent glioblastoma. Neurologia medico-chirurgica 54: 302–309.CrossRef
38.
go back to reference Fahrendorf D, Hesselmann V, Schwindt W, Wolfer J, Jeibmann A, Kooijman H, Kugel H, Heindel W, Bink A (2015) Variations of ITSS-morphology and their relationship to location and tumor volume in patients with glioblastoma. J Neuroimag. doi:10.1111/jon.12228 CrossRef Fahrendorf D, Hesselmann V, Schwindt W, Wolfer J, Jeibmann A, Kooijman H, Kugel H, Heindel W, Bink A (2015) Variations of ITSS-morphology and their relationship to location and tumor volume in patients with glioblastoma. J Neuroimag. doi:10.​1111/​jon.​12228 CrossRef
Metadata
Title
Decreased survival in glioblastomas is specific to contact with the ventricular-subventricular zone, not subgranular zone or corpus callosum
Authors
Akshitkumar M. Mistry
Michael C. Dewan
Gabrielle A. White-Dzuro
Philip R. Brinson
Kyle D. Weaver
Reid C. Thompson
Rebecca A. Ihrie
Lola B. Chambless
Publication date
01-04-2017
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2017
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-017-2374-3

Other articles of this Issue 2/2017

Journal of Neuro-Oncology 2/2017 Go to the issue