Top

Published in:

01-01-2017 | Clinical Study

Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis

Authors: Akshitkumar M. Mistry, Andrew T. Hale, Lola B. Chambless, Kyle D. Weaver, Reid C. Thompson, Rebecca A. Ihrie

Published in: Journal of Neuro-Oncology | Issue 1/2017

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.

Available only for authorised users

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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, 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

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

10.

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 CrossRefPubMedPubMedCentral

11.

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 CrossRefPubMed

12.

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

13.

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

14.

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 CrossRefPubMed

15.

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.

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 CrossRefPubMedPubMedCentral

17.

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 CrossRefPubMedPubMedCentral

18.

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 CrossRefPubMed

19.

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 CrossRefPubMed

20.

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: 302–309CrossRefPubMed

21.

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 CrossRefPubMed

22.

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 CrossRefPubMed

23.

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

24.

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 CrossRefPubMed

25.

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 53:52–59CrossRefPubMed

26.

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 CrossRefPubMedPubMedCentral

27.

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 CrossRefPubMedPubMedCentral

28.

Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions. The Cochrane Collaboration. Wiley-Blackwell: Chichester

29.

Machin D, Cheung YB, Parmar M (2006) Survival analysis: A practical approach. Wiley

30.

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 CrossRefPubMedPubMedCentral

31.

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 CrossRefPubMedPubMedCentral

32.

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 CrossRefPubMedPubMedCentral

33.

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

34.

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 CrossRefPubMed

35.

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 CrossRefPubMedPubMedCentral

36.

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 CrossRefPubMedPubMedCentral

37.

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)CrossRefPubMedPubMedCentral

38.

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 CrossRefPubMedPubMedCentral

39.

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

40.

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

41.

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

42.

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 CrossRefPubMedPubMedCentral

43.

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 CrossRefPubMed

44.

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 CrossRefPubMed

45.

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 CrossRefPubMed

46.

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

47.

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 PubMed

48.

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 CrossRefPubMedPubMedCentral

49.

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 CrossRefPubMed

50.

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 CrossRefPubMed

Title: Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis
Authors: Akshitkumar M. Mistry
Andrew T. Hale
Lola B. Chambless
Kyle D. Weaver
Reid C. Thompson
Rebecca A. Ihrie
Publication date: 01-01-2017
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 1/2017
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-016-2278-7

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2017

Impact of operative length on post-operative complications in meningioma surgery: a NSQIP analysis

In vivo molecular profiling of human glioma using diffusion kurtosis imaging

Jab1 promotes glioma cell proliferation by regulating Siah1/β-catenin pathway

Incidence, time trends and survival patterns of childhood pilocytic astrocytomas in Southern-Eastern Europe and SEER, US

Analyses of prognosis-related factors of intracranial solitary fibrous tumors and hemangiopericytomas help understand the relationship between the two sorts of tumors

Preliminary experience of the concurrent use of radiosurgery and T-DM1 for brain metastases in HER2-positive metastatic breast cancer