Abstract
The ventricular-subventricular zone (V-SVZ), which lies in the walls of the lateral ventricles (LV), is the largest neurogenic niche within the adult brain. Whether radiographic contact with the LV influences survival in glioblastoma (GBM) patients remains unclear. We assimilated and analyzed published data comparing survival in GBM patients with (LV+GBM) and without (LV-GBM) radiographic LV contact. PubMed, EMBASE, and Cochrane electronic databases were searched. Fifteen studies with survival data on LV+GBM and LV-GBM patients were identified. Their Kaplan–Meier survival curves were digitized and pooled for generation of median overall (OS) and progression free (PFS) survivals and log-rank hazard ratios (HRs). The log-rank and reported multivariate HRs after accounting for the common predictors of GBM survival were analyzed separately by meta-analyses. The calculated median survivals (months) from pooled data were 12.95 and 16.58 (OS), and 4.54 and 6.25 (PFS) for LV+GBMs and LV-GBMs, respectively, with an overall log-rank HRs of 1.335 [1.204–1.513] (OS) and 1.387 [1.225–1.602] (PFS). Meta-analysis of log-rank HRs resulted in summary HRs of 1.58 [1.35–1.85] (OS, 10 studies) and 1.41 [1.22–1.64] (PFS, 5 studies). Meta-analysis of multivariate HRs resulted in summary HRs of 1.35 [1.14–1.58] (OS, 6 studies) and 1.64 [0.88–3.05] (PFS, 3 studies). Patients with GBM contacting the LV have lower survival. This effect may be independent of the common predictors of GBM survival, suggesting a clinical influence of V-SVZ contact on GBM biology.
Similar content being viewed by others
References
Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, Jeraj R, Brown PD, Jaeckle KA, Schiff D, Stieber VW, Brachman DG, Werner-Wasik M, Tremont-Lukats IW, Sulman EP, Aldape KD, Curran WJ Jr, Mehta MP (2014) A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 370:699–708. doi:10.1056/NEJMoa1308573
Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, Brandes AA, Hilton M, Abrey L, Cloughesy T (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722. doi:10.1056/NEJMoa1308345
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760. doi:10.1038/nature05236
Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF (2012) A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488:522–526. doi:10.1038/nature11287
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
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
Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249. doi:10.1126/science.1136281
Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisen J (2014) Neurogenesis in the striatum of the adult human brain. Cell 156:1072–1083. doi:10.1016/j.cell.2014.01.044
Lim DA, Cha S, Mayo MC, Chen MH, Keles E, VandenBerg S, Berger MS (2007) Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro-oncol 9:424–429. doi:10.1215/15228517-2007-023
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6:e1000097. doi:10.1371/journal.pmed.1000097
Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A (2008) Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol 89:219–224. doi:10.1007/s11060-008-9609-2
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
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
Young GS, Macklin EA, Setayesh K, Lawson JD, Wen PY, Norden AD, Drappatz J, Kesari S (2011) Longitudinal MRI evidence for decreased survival among periventricular glioblastoma. J Neurooncol 104:261–269. doi:10.1007/s11060-010-0477-1
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)
Chaichana KL, Pendleton C, Chambless L, Camara-Quintana J, Nathan JK, Hassam-Malani L, Li G, Harsh GRt, 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
Ho J, Ondos J, Ning H, Smith S, Kreisl T, Iwamoto F, Sul J, Kim L, McNeil K, Krauze A, Shankavaram U, Fine HA, Camphausen K (2013) Chemoirradiation for glioblastoma multiforme: the national cancer institute experience. PloS One 8:e70745. doi:10.1371/journal.pone.0070745
Jafri NF, Clarke JL, Weinberg V, Barani IJ, Cha S (2013) Relationship of glioblastoma multiforme to the subventricular zone is associated with survival. Neuro-oncol 15:91–96. doi:10.1093/neuonc/nos268
Adeberg S, Konig L, Bostel T, Harrabi S, Welzel T, Debus J, Combs SE (2014) Glioblastoma recurrence patterns after radiation therapy with regard to the subventricular zone. Int J Radiat Oncol Biol Phys 90:886–893. doi:10.1016/j.ijrobp.2014.07.027
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
Tomita T, Akimoto J, Haraoka J, Kudo M (2014) Clinicopathological significance of expression of nestin, a neural stem/progenitor cell marker, in human glioma tissue. Brain Tumor Pathol 31:162–171. doi:10.1007/s10014-013-0169-6
Han S, Li X, Qiu B, Jiang T, Wu A (2015) Can lateral ventricle contact predict the ontogeny and prognosis of glioblastoma? J Neurooncol 124:45–55. doi:10.1007/s11060-015-1818-x
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: J Eur Soc Ther Radiol Int Soc Cell. doi:10.1016/j.radonc.2015.11.017
Nestler U, Lutz K, Pichlmeier U, Stummer W, Franz K, Reulen HJ, Bink A, Group ALAGS (2015) Anatomic features of glioblastoma and their potential impact on survival. Acta neurochirurgica 157: 179–186. doi:10.1007/s00701-014-2271-x
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 Neuropathol 53:52–59
Wan X, Peng L, Li Y (2015) A review and comparison of methods for recreating individual patient data from published Kaplan–Meier survival curves for economic evaluations: a simulation study. PloS One 10:e0121353. doi:10.1371/journal.pone.0121353
Guyot P, Ades AE, Ouwens MJ, Welton NJ (2012) Enhanced secondary analysis of survival data: reconstructing the data from published Kaplan–Meier survival curves. BMC Med Res Methodol 12:9. doi:10.1186/1471-2288-12-9
Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions. The Cochrane Collaboration. Wiley-Blackwell: Chichester
Machin D, Cheung YB, Parmar M (2006) Survival analysis: A practical approach. Wiley
Galvao RP, Kasina A, McNeill RS, Harbin JE, Foreman O, Verhaak RG, Nishiyama A, Miller CR, Zong H (2014) Transformation of quiescent adult oligodendrocyte precursor cells into malignant glioma through a multistep reactivation process. Proc Natl Acad Sci USA 111:E4214–E4223. doi:10.1073/pnas.1414389111
Alcantara Llaguno SR, Wang Z, Sun D, Chen J, Xu J, Kim E, Hatanpaa KJ, Raisanen JM, Burns DK, Johnson JE, Parada LF (2015) Adult lineage-restricted CNS progenitors specify distinct glioblastoma subtypes. Cancer Cell 28:429–440. doi:10.1016/j.ccell.2015.09.007
Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, Zong H (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146:209–221. doi:10.1016/j.cell.2011.06.014
Zong H, Parada LF, Baker SJ (2015) Cell of origin for malignant gliomas and its implication in therapeutic development. Cold Spring Harbor Perspectives Biol 7. doi:10.1101/cshperspect.a020610
Kusne Y, Sanai N (2015) The SVZ and its relationship to stem cell based neuro-oncogenesis. Adv Exp Med Biol 853:23–32. doi:10.1007/978-3-319-16537-0_2
Marumoto T, Tashiro A, Friedmann-Morvinski D, Scadeng M, Soda Y, Gage FH, Verma IM (2009) Development of a novel mouse glioma model using lentiviral vectors. Nat Med 15:110–116. doi:10.1038/nm.1863
Friedmann-Morvinski D, Bushong EA, Ke E, Soda Y, Marumoto T, Singer O, Ellisman MH, Verma IM (2012) Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338:1080–1084. doi:10.1126/science.1226929
Bohman LE, Swanson KR, Moore JL, Rockne R, Mandigo C, Hankinson T, Assanah M, Canoll P, Bruce JN (2010) Magnetic resonance imaging characteristics of glioblastoma multiforme: implications for understanding glioma ontogeny. Neurosurgery 67:1319–1327. doi:10.1227/NEU.0b013e3181f556ab (discussion 1327–1318)
Haskins WE, Zablotsky BL, Foret MR, Ihrie RA, Alvarez-Buylla A, Eisenman RN, Berger MS, Lin CH (2013) Molecular Characteristics in MRI-Classified Group 1 Glioblastoma Multiforme. Front Oncol 3:182. doi:10.3389/fonc.2013.00182
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
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
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
Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY (2000) Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 97:12846–12851. doi:10.1073/pnas.97.23.12846
Ziu M, Schmidt NO, Cargioli TG, Aboody KS, Black PM, Carroll RS (2006) Glioma-produced extracellular matrix influences brain tumor tropism of human neural stem cells. J Neurooncol 79:125–133. doi:10.1007/s11060-006-9121-5
Zhao D, Najbauer J, Garcia E, Metz MZ, Gutova M, Glackin CA, Kim SU, Aboody KS (2008) Neural stem cell tropism to glioma: critical role of tumor hypoxia. Mol Cancer Res: MCR 6:1819–1829. doi:10.1158/1541-7786.mcr-08-0146
Capilla-Gonzalez V, Lavell E, Quinones-Hinojosa A, Guerrero-Cazares H (2015) Regulation of subventricular zone-derived cells migration in the adult brain. Adv Exp Med Biol 853:1–21. doi:10.1007/978-3-319-16537-0_1
Berendsen S, Schoysman L, Kroonen J, Hendrikse J, Seute T, Spliet WGM, Poulet C, Bours V, Robe PA (2015) Glioblastoma involving the subventricular zone: correlations to patient survival and tumor biology. Abstracts from the 20th Annual Scientific Meeting of the Society for Neuro-Oncology. Oxford University Press, San Antonio, p v79
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 Neuroimaging. doi:10.1111/jon.12228
Chen L, Guerrero-Cazares H, Ye X, Ford E, McNutt T, Kleinberg L, Lim M, Chaichana K, Quinones-Hinojosa A, Redmond K (2013) Increased subventricular zone radiation dose correlates with survival in glioblastoma patients after gross total resection. Int J Radiat Oncol Biol Phys 86:616–622. doi:10.1016/j.ijrobp.2013.02.014
Lee P, Eppinga W, Lagerwaard F, Cloughesy T, Slotman B, Nghiemphu PL, Wang PC, Kupelian P, Agazaryan N, Demarco J, Selch MT, Steinberg M, Kang JJ (2013) Evaluation of high ipsilateral subventricular zone radiation therapy dose in glioblastoma: a pooled analysis. Int J Radiat Oncol Biol Phys 86:609–615. doi:10.1016/j.ijrobp.2013.01.009
Elicin O, Inac E, Uzel EK, Karacam S, Uzel OE (2014) Relationship between survival and increased radiation dose to subventricular zone in glioblastoma is controversial. J Neurooncol 118:413–419. doi:10.1007/s11060-014-1424-3
Acknowledgements
We thank Dr. Tseng for providing unpublished Kaplan–Meier survival curves of LV+GBM and LV-GBM patient data analyzed in the study Liang et al. [22].
Funding
This work was by supported a grant from the Institute for Clinical and Translational Research, Vanderbilt University, part of the National Center for Advancing Translational Sciences, CTSA award No. UL1TR000445 (A.M.M.) and Discovery Grants from the Vanderbilt-Ingram Cancer Center (R.A.I.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mistry, A.M., Hale, A.T., Chambless, L.B. et al. Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis. J Neurooncol 131, 125–133 (2017). https://doi.org/10.1007/s11060-016-2278-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-016-2278-7