Abstract
Purpose
Leptomeningeal spread to the fourth ventricle (LSFV) from supratentorial high-grade astrocytoma (HGA) is rarely investigated. The incidence and prognostic merit of LSFV were analyzed in this study.
Methods
A consecutive cohort of 175 patients with pathologically diagnosed HGA according to the 2016 WHO classification of brain tumors was enrolled. LSFV was defined as radiological occupation in the fourth ventricle at the moment of initial progression. Clinical, radiological, and pathological data were analyzed to explore the difference between HGA patients with and without LSFV.
Results
There were 18 of 175 (10.3%) HGAs confirmed with LSFV. The difference of survival rate between patients with LSFV or not was significant in both overall survival (OS) (14.5 vs. 24 months, P = 0.0007) and post progression survival (PPS) (6.0 vs. 11.5 months, P = 0.0004), while no significant difference was observed in time to progression (TTP) (8.5 months vs. 9.5 months P = 0.6795). In the Cox multivariate analysis, LSFV was confirmed as an independent prognostic risk factor for OS (HR 2.06, P = 0.010). LSFV was correlated with younger age (P = 0.044), ventricle infringement of primary tumor (P < 0.001) and higher Ki-67 index (P = 0.013) in further analysis, and the latter two have been validated in the Logistic regression analysis (OR 18.16, P = 0.006; OR 4.04, P = 0.012, respectively).
Conclusion
LSFV was indicative of end-stage for supratentorial HGA patients, which shortened patients’ PPS and OS instead of TTP. It’s never too cautious to alert this lethal event when tumor harbored ventricle infringement and higher Ki-67 index in routine clinical course.
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References
Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359(5):492–507
Behin A, Hoang-Xuan K, Carpentier AF, Delattre JY (2003) Primary brain tumours in adults. Lancet 361(9354):323–331. https://doi.org/10.1016/s0140-6736(03)12328-8
Rick J, Chandra A, Aghi MK (2018) Tumor treating fields: a new approach to glioblastoma therapy. J Neurooncol. https://doi.org/10.1007/s11060-018-2768-x
Lim M, Xia Y, Bettegowda C, Weller M (2018) Current state of immunotherapy for glioblastoma. Nat Rev Clin Oncol 15(7):422–442. https://doi.org/10.1038/s41571-018-0003-5
Weathers SS, Gilbert MR (2017) Toward personalized targeted therapeutics: an overview. Neurotherapeutics 14(2):256–264. https://doi.org/10.1007/s13311-016-0496-5
Pope WB, Xia Q, Paton VE, Das A, Hambleton J, Kim HJ, Huo J, Brown MS, Goldin J, Cloughesy T (2011) Patterns of progression in patients with recurrent glioblastoma treated with bevacizumab. Neurology 76(5):432–437
Fujimura M, Kumabe T, Jokura H, Shirane R, Yoshimoto T, Tominaga T (2004) Intractable vomiting as an early clinical symptom of cerebrospinal fluid seeding to the fourth ventricle in patients with high-grade astrocytoma. J Neuro-Oncol 66(1–2):209–216
Burger MC, Zeiner PS, Jahnke K, Wagner M, Mittelbronn M, Steinbach JP (2016) Addition of anti-angiogenetic therapy with bevacizumab to chemo- and radiotherapy for leptomeningeal metastases in primary brain tumors. PLoS ONE 11(6):e0155315. https://doi.org/10.1371/journal.pone.0155315
Zhang Z, Jiang H, Chen X, Bai J, Cui Y, Ren X, Chen X, Wang J, Zeng W, Lin S (2014) Identifying the survival subtypes of glioblastoma by quantitative volumetric analysis of MRI. J Neurooncol 119(1):207–214. https://doi.org/10.1007/s11060-014-1478-2
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(4):424–429
Kuhnt D, Becker A, Ganslandt O, Bauer M, Buchfelder M, Nimsky C (2011) Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol 13(12):1339–1348. https://doi.org/10.1093/neuonc/nor133
Jiang H, Cui Y, Liu X, Ren X, Lin S (2017) Patient-specific resection strategy of glioblastoma multiforme: choice based on a preoperative scoring scale. Ann Surg Oncol 24(7):2006–2014. https://doi.org/10.1245/s10434-017-5843-1
Iwamoto FM, Abrey LE, Beal K, Gutin PH, Rosenblum MK, Reuter VE, Deangelis LM, Lassman AB (2009) Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma. Neurology 73(15):1239–1241
Jiang H, Zhang Z, Ren X, Zeng W, Jia W, Wang J, Lin S (2014) 1p/19q-driven prognostic molecular classification for high-grade oligodendroglial tumors. J Neurooncol 120(3):607–614. https://doi.org/10.1007/s11060-014-1593-0
Jiang H, Ren X, Wang J, Zhang Z, Jia W, Lin S (2014) Short-term survivors in glioblastomas with oligodendroglioma component: a clinical study of 186 Chinese patients from a single institution. J Neurooncol 116(2):395–404. https://doi.org/10.1007/s11060-013-1311-3
Cai X, Qin JJ, Hao SY, Li H, Zeng C, Sun SJ, Yu LB, Gao ZX, Xie J (2018) Clinical characteristics associated with the intracranial dissemination of gliomas. Clin Neurol Neurosurg 166:141–146. https://doi.org/10.1016/j.clineuro.2018.01.038
Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, Degroot J, Wick W, Gilbert MR, Lassman AB, Tsien C, Mikkelsen T, Wong ET, Chamberlain MC, Stupp R, Lamborn KR, Vogelbaum MA, van den Bent MJ, Chang SM (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28(11):1963–1972. https://doi.org/10.1200/jco.2009.26.3541
Cohen ZR, Hassenbusch SJ, Maor MH, Pfeffer RM, Ram Z (2002) Intractable vomiting from glioblastoma metastatic to the fourth ventricle: three case studies. Neuro-Oncology 4(2):129–133
Khan MN, Poulin A, Essig M (2017) Fourth Ventricular lesions in metastatic gliomas: a rare predilection? Brain Tumor Res Treat 5(1):24–29. https://doi.org/10.14791/btrt.2017.5.1.24
de Groot JF, Fuller G, Kumar AJ, Piao Y, Eterovic K, Ji Y, Conrad CA (2010) Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro-oncology 12(3):233
Arita N, Taneda M, Hayakawa T (1994) Leptomeningeal dissemination of malignant gliomas. Incidence, diagnosis and outcome. Acta Neurochir (Wien) 126(2–4):84–92
Noh JH, Lee MH, Kim WS, Lim DH, Kim ST, Kong DS, Nam DH, Lee JI, Seol HJ (2015) Optimal treatment of leptomeningeal spread in glioblastoma: analysis of risk factors and outcome. Acta Neurochir (Wien) 157(4):569–576. https://doi.org/10.1007/s00701-015-2344-5
Matsuda M, Kohzuki H, Ishikawa E, Yamamoto T, Akutsu H, Takano S, Mizumoto M, Tsuboi K, Matsumura A (2018) Prognostic analysis of patients who underwent gross total resection of newly diagnosed glioblastoma. J Clin Neurosci 50:172–176. https://doi.org/10.1016/j.jocn.2018.01.009
Gai X, Li S, Wei Y, Yu S (2018) A case report about oligodendrogliomas of the fourth ventricle. Med (Baltimore) 97(17):e0594. https://doi.org/10.1097/MD.0000000000010594
Perry JR, Laperriere N, Mason WP (2017) Radiation plus temozolomide in patients with glioblastoma. N Engl J Med 376(22):2197. https://doi.org/10.1056/NEJMc1704726
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(8):699–708. https://doi.org/10.1056/NEJMoa1308573
Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360(8):765–773. https://doi.org/10.1056/NEJMoa0808710
Baker H (2015) Radiotherapy in the elderly and frail with glioblastoma. Lancet Oncol 16(15):e530. https://doi.org/10.1016/s1470-2045(15)00371-x
VandenDriessche T, Chuah MK (2013) Glioblastoma: bridging the gap with gene therapy. Lancet Oncol 14(9):789–790. https://doi.org/10.1016/s1470-2045(13)70342-5
Okawa S, Gagrica S, Blin C, Ender C, Pollard SM, Krijgsveld J (2017) Proteome and secretome characterization of glioblastoma-derived neural stem cells. Stem cells (Dayton Ohio) 35(4):967–980. https://doi.org/10.1002/stem.2542
Qin EY, Cooper DD, Abbott KL, Lennon J, Nagaraja S, Mackay A, Jones C, Vogel H, Jackson PK, Monje M (2017) Neural precursor-derived pleiotrophin mediates subventricular zone invasion by glioma. Cell 170(5):845–859 e819. https://doi.org/10.1016/j.cell.2017.07.016
Goffart N, Lombard A, Lallemand F, Kroonen J, Nassen J, Di Valentin E, Berendsen S, Dedobbeleer M, Willems E, Robe P, Bours V, Martin D, Martinive P, Maquet P, Rogister B (2017) CXCL12 mediates glioblastoma resistance to radiotherapy in the subventricular zone. Neuro-Oncology 19(1):66–77. https://doi.org/10.1093/neuonc/now136
Roelz R, Reinacher P, Jabbarli R, Kraeutle R, Hippchen B, Egger K, Weyerbrock A, Machein M (2015) Surgical Ventricular entry is a key risk factor for leptomeningeal metastasis of high grade gliomas. Sci Rep 5:17758. https://doi.org/10.1038/srep17758
Mistry AM, Kelly PD, Thompson RC, Chambless LB (2018) Cancer dissemination, hydrocephalus, and survival after cerebral ventricular entry during high-grade glioma surgery: a meta-analysis. Neurosurgery. https://doi.org/10.1093/neuros/nyy202
Li Y, Qian Z, Xu K, Wang K, Fan X, Li S, Liu X, Wang Y, Jiang T (2017) Radiomic features predict Ki-67 expression level and survival in lower grade gliomas. J Neurooncol 135(2):317–324. https://doi.org/10.1007/s11060-017-2576-8
Rezai AR, Woo HH, Lee M, Cohen H, Zagzag D, Epstein FJ (1996) Disseminated ependymomas of the central nervous system. J Neurosurg 85(4):618–624. https://doi.org/10.3171/jns.1996.85.4.0618
Kato H, Fujimura M, Kumabe T, Ishioka C, Kanamaru R, Yoshimoto T (2004) PTEN gene mutation and high MIB-1 labeling index may contribute to dissemination in patients with glioblastoma. J Clin Neurosci 11(1):37–41. https://doi.org/10.1016/j.jocn.2002.09.001
Pasquale DB, Carmelo A, Angelo P, Alba F, Mario B, Silvia C, Libero L, Giulio M, Annunziato MJCN (2013) The influence of surgery on recurrence pattern of glioblastoma. Neurosurgery 115(1):37–43
Rapp M, Baernreuther J, Turowski B, Steiger HJ, Sabel M, Kamp MA (2017) Recurrence pattern analysis of primary glioblastoma. World Neurosurg 103:733–740. https://doi.org/10.1016/j.wneu.2017.04.053
Burger MC, Ronellenfitsch MW, Lorenz NI, Wagner M, Voss M, Capper D, Tzaridis T, Herrlinger U, Steinbach JP, Stoffels G, Langen KJ, Brandts C, Senft C, Harter PN, Bahr O (2017) Dabrafenib in patients with recurrent, BRAF V600E mutated malignant glioma and leptomeningeal disease. Oncol Rep 38(6):3291–3296. https://doi.org/10.3892/or.2017.6013
Nandipati S, Demopoulos A (2011) Leptomeningeal dissemination of anaplastic glioma: prolonged survival in two patients treated with temozolomide. J Neurooncol 105(3):663–665. https://doi.org/10.1007/s11060-011-0611-8
Smith JS, Parney IF, Lamborn KR, Mcdermott MW, Sneed PK, Chang SM (2007) Treatment for posterior fossa dissemination of primary supratentorial glioma. J Neurosurg 106(4):567–574
Okita Y, Nonaka M, Umehara T, Kanemura Y, Kodama Y, Mano M, Nakajima S (2015) Efficacy of temozolomide and bevacizumab for the treatment of leptomeningeal dissemination of recurrent glioblastoma: a case report. Oncol Lett 9(4):1885–1888. https://doi.org/10.3892/ol.2015.2940
Linsenmann T, Monoranu CM, Vince GH, Westermaier T, Hagemann C, Kessler AF, Ernestus RI, Lohr M (2014) Long-term tumor control of spinal dissemination of cerebellar glioblastoma multiforme by combined adjuvant bevacizumab antibody therapy: a case report. BMC Res Notes 7:496. https://doi.org/10.1186/1756-0500-7-496
Acknowledgements
It’s extremely precious that the patients rigorously performed every follow-up in our department, which provided us accurate materials for this analysis. The authors sincerely thank the patients and their families for their participation in the present study.
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This study was funded by National Natural Science Foundation of China (81571632).
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Capital Medical University and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Li, M., Ren, X., Jiang, H. et al. Supratentorial high-grade astrocytoma with leptomeningeal spread to the fourth ventricle: a lethal dissemination with dismal prognosis. J Neurooncol 142, 253–261 (2019). https://doi.org/10.1007/s11060-018-03086-8
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DOI: https://doi.org/10.1007/s11060-018-03086-8