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

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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.

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References

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. Vescovi AL, Galli R, Reynolds BA (2006) Brain tumour stem cells. Nature Rev Cancer 6:425–436. doi:10.1038/nrc1889

    Article  CAS  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. Mickevicius NJ, Carle AB, Bluemel T, Santarriaga S, Schloemer F, Shumate D, Connelly J, Schmainda KM, LaViolette PS (2015) Location of brain tumor intersecting white matter tracts predicts patient prognosis. J Neurooncol 125:393–400. doi:10.1007/s11060-015-1928-5

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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)

    Article  PubMed  Google Scholar 

  11. 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

    Article  PubMed  PubMed Central  Google Scholar 

  12. Mistry AM, Hale AT, Chambless LB, Weaver KD, Thompson RC, Ihrie RA (2016) Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis. J Neurooncol. doi:10.1007/s11060-016-2278-7

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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 Neurochir 157:179–186. doi:10.1007/s00701-014-2271-x

    Article  CAS  PubMed  Google Scholar 

  23. 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.

    Article  CAS  Google Scholar 

  24. Chen L, Chaichana KL, Kleinberg L, Ye X, Quinones-Hinojosa A, Redmond K (2015) Glioblastoma recurrence patterns near neural stem cell regions. Radiother Oncol. doi:10.1016/j.radonc.2015.07.032

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Google Scholar 

  26. Bredel M (2008) Nomograms as clinicobiological predictors of survival in glioblastoma. The Lancet Oncol 9:5–6. doi:10.1016/s1470-2045(07)70390-x

    Article  PubMed  Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. Gage FH, Temple S (2013) Neural stem cells: generating and regenerating the brain. Neuron 80:588–601. doi:10.1016/j.neuron.2013.10.037

    Article  CAS  PubMed  Google Scholar 

  29. Gilbertson RJ, Rich JN (2007) Making a tumour’s bed: glioblastoma stem cells and the vascular niche. Nature Rev Cancer 7:733–736. doi:10.1038/nrc2246

    Article  CAS  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. Ernst A, Frisen J (2015) Adult neurogenesis in humans- common and unique traits in mammals. PLoS Biol 13: e1002045. doi:10.1371/journal.pbio.1002045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. Parsa AT, Wachhorst S, Lamborn KR, Prados MD, McDermott MW, Berger MS, Chang SM (2005) Prognostic significance of intracranial dissemination of glioblastoma multiforme in adults. J Neurosurg 102:622–628. doi:10.3171/jns.2005.102.4.0622

    Article  PubMed  Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. 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.

    Article  Google Scholar 

  37. Barami K, Sloan AE, Rojiani A, Schell MJ, Staller A, Brem S (2009) Relationship of gliomas to the ventricular walls. J Clin Neurosci 16:195–201. doi:10.1016/j.jocn.2008.03.006

    Article  PubMed  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. Faissner A, Reinhard J (2015) The extracellular matrix compartment of neural stem and glial progenitor cells. Glia 63:1330–1349. doi:10.1002/glia.22839

    Article  PubMed  Google Scholar 

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Funding

Vanderbilt Institute for Clinical and Translational Research grant support from the National Center for Advancing Translational Sciences [CTSA award No. UL1TR000445 to AMM]; Vanderbilt-Ingram Cancer Center Ambassadors, Vanderbilt-Ingram Cancer Center Discovery Grant, and National Institutes of Health [Cancer Center Support Grant P30 CA068485 and NINDS R01096238 to RAI]. We acknowledge Li Wang and Dr. Chang Yu of Vanderbilt Department of Biostatistics for statistical guidance.

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Authors and Affiliations

  1. Department of Neurological Surgery, Vanderbilt University Medical Center, T-4224 Medical Center North, 1161 21st Avenue South, Nashville, TN, 37232-2380, USA

    Akshitkumar M. Mistry, Michael C. Dewan, Philip R. Brinson, Kyle D. Weaver, Reid C. Thompson, Rebecca A. Ihrie & Lola B. Chambless

  2. School of Medicine, Vanderbilt University, Nashville, TN, USA

    Gabrielle A. White-Dzuro

  3. Department of Cancer Biology, Vanderbilt University, Nashville, TN, USA

    Rebecca A. Ihrie

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  1. Akshitkumar M. Mistry
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Correspondence to Akshitkumar M. Mistry.

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Mistry, A.M., Dewan, M.C., White-Dzuro, G.A. et al. Decreased survival in glioblastomas is specific to contact with the ventricular-subventricular zone, not subgranular zone or corpus callosum. J Neurooncol 132, 341–349 (2017). https://doi.org/10.1007/s11060-017-2374-3

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