Ventricular entry during surgical resection is associated with intracranial leptomeningeal dissemination in glioblastoma patients.
Glioblastoma
Leptomeningeal dissemination
Ventricular entry
Journal
Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
30
07
2022
accepted:
12
10
2022
pubmed:
24
10
2022
medline:
15
12
2022
entrez:
23
10
2022
Statut:
ppublish
Résumé
Glioblastoma (GBM) is associated with a poorer prognosis when leptomeningeal dissemination (LMD) occurs. Recently, the role of both ventricular entry (VE) during surgery and subventricular zone localization of tumors in promoting LMD in GBM patients has been debated. This article investigates the role of VE in causing LMD in GBM patients. We conducted a retrospective analysis of GBMs operated on at our Institution between March 2018 and December 2020. We collected pre- and post-surgical images, anamnestic information, and surgical reports. Two hundred cases were collected. The GBM localization was periventricular in 69.5% of cases, and there was a VE during the surgical procedure in 51% of cases. The risk of post-surgical LMD in the case of VE was 16%. The rate of LMD was higher in the case of VE than not-VE (27.4% vs. 4%, p < 0.0001). The rate of LMD in periventricular GBM was 19% (p = 0.1131). According to our data, VE is an independent factor associated with a higher rate of post-surgical LMD, and the periventricular localization is not independently correlated to this negative outcome. Neurosurgeons should avoid VE when possible. The correct surgical strategy should be founded on balancing the need for maximal EOR and the risks associated with VE.
Identifiants
pubmed: 36273377
doi: 10.1007/s11060-022-04166-6
pii: 10.1007/s11060-022-04166-6
pmc: PMC9722854
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
473-480Informations de copyright
© 2022. The Author(s).
Références
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492
doi: 10.3322/caac.21492
pubmed: 30207593
Wirsching HG, Galanis E, Weller M (2016) Glioblastoma. Handb Clin Neurol 134:381–397. https://doi.org/10.1016/b978-0-12-802997-8.00023-2
doi: 10.1016/b978-0-12-802997-8.00023-2
pubmed: 26948367
Davis ME (2016) Glioblastoma: overview of disease and treatment. Clin J Oncol Nurs 20:S2-8. https://doi.org/10.1188/16.Cjon.S1.2-8
doi: 10.1188/16.Cjon.S1.2-8
pubmed: 27668386
pmcid: 5123811
Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS, Villano JL (2014) Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev 23:1985–1996. https://doi.org/10.1158/1055-9965.Epi-14-0275
doi: 10.1158/1055-9965.Epi-14-0275
pubmed: 25053711
pmcid: 4185005
Wright CH, Wright J, Onyewadume L, Raghavan A, Lapite I, Casco-Zuleta A, Lagman C, Sajatovic M, Hodges TR (2019) Diagnosis, treatment, and survival in spinal dissemination of primary intracranial glioblastoma: systematic literature review. J Neurosurg Spine. https://doi.org/10.3171/2019.5.Spine19164
doi: 10.3171/2019.5.Spine19164
pubmed: 31675723
Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003. https://doi.org/10.1056/NEJMoa043331
doi: 10.1056/NEJMoa043331
pubmed: 15758010
Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62: 564–576; discussion 564–576. https://doi.org/10.1227/01.neu.0000317304.31579.17
Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, Taylor LP, Lieberman F, Silvani A, Fink KL, Barnett GH, Zhu JJ, Henson JW, Engelhard HH, Chen TC, Tran DD, Sroubek J, Tran ND, Hottinger AF, Landolfi J, Desai R, Caroli M, Kew Y, Honnorat J, Idbaih A, Kirson ED, Weinberg U, Palti Y, Hegi ME, Ram Z (2015) Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA 314:2535–2543. https://doi.org/10.1001/jama.2015.16669
doi: 10.1001/jama.2015.16669
pubmed: 26670971
Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198. https://doi.org/10.3171/jns.2001.95.2.0190
doi: 10.3171/jns.2001.95.2.0190
pubmed: 11780887
Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, Patel AS, Rizk EB, Suki D, Sawaya R, Glantz M (2016) Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol 2:1460–1469. https://doi.org/10.1001/jamaoncol.2016.1373
doi: 10.1001/jamaoncol.2016.1373
pubmed: 27310651
pmcid: 6438173
Sanai N, Berger MS (2018) Surgical oncology for gliomas: the state of the art. Nat Rev Clin Oncol 15:112–125. https://doi.org/10.1038/nrclinonc.2017.171
doi: 10.1038/nrclinonc.2017.171
pubmed: 29158591
Hallaert G, Pinson H, Van den Broecke C, Vanhauwaert D, Van Roost D, Boterberg T, Kalala JP (2020) Subventricular zone contacting glioblastoma: tumor size, molecular biological factors and patient survival. Acta Oncol (Stockholm, Sweden) 59:1474–1479. https://doi.org/10.1080/0284186x.2020.1794032
doi: 10.1080/0284186x.2020.1794032
Ahmadipour Y, Jabbarli R, Gembruch O, Pierscianek D, Darkwah Oppong M, Dammann P, Wrede K, Özkan N, Müller O, Sure U, El Hindy N (2019) Impact of multifocality and molecular markers on survival of glioblastoma. World Neurosurg 122:e461–e466. https://doi.org/10.1016/j.wneu.2018.10.075
doi: 10.1016/j.wneu.2018.10.075
pubmed: 30347300
Arita N, Taneda M, Hayakawa T (1994) Leptomeningeal dissemination of malignant gliomas. Incidence, diagnosis and outcome. Acta Neurochir 126:84–92. https://doi.org/10.1007/bf01476415
doi: 10.1007/bf01476415
pubmed: 8042560
Jiang H, Yu K, Li M, Cui Y, Ren X, Yang C, Zhao X, Lin S (2020) Classification of progression patterns in glioblastoma: analysis of predictive factors and clinical implications. Front Oncol 10:590648. https://doi.org/10.3389/fonc.2020.590648
doi: 10.3389/fonc.2020.590648
pubmed: 33251147
pmcid: 7673412
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 83:1119–1127. https://doi.org/10.1093/neuros/nyy202
doi: 10.1093/neuros/nyy202
pubmed: 29790976
Mandel JJ, Yust-Katz S, Cachia D, Wu J, Liu D, de Groot JF, Yung AW, Gilbert MR (2014) Leptomeningeal dissemination in glioblastoma; an inspection of risk factors, treatment, and outcomes at a single institution. J Neurooncol 120:597–605. https://doi.org/10.1007/s11060-014-1592-1
doi: 10.1007/s11060-014-1592-1
pubmed: 25168214
Elliott JP, Keles GE, Waite M, Temkin N, Berger MS (1994) Ventricular entry during resection of malignant gliomas: effect on intracranial cerebrospinal fluid tumor dissemination. J Neurosurg 80:834–839. https://doi.org/10.3171/jns.1994.80.5.0834
doi: 10.3171/jns.1994.80.5.0834
pubmed: 8169622
Grabb PA, Albright AL, Pang D (1992) Dissemination of supratentorial malignant gliomas via the cerebrospinal fluid in children. Neurosurgery 30:64–71. https://doi.org/10.1227/00006123-199201000-00012
doi: 10.1227/00006123-199201000-00012
pubmed: 1738457
Young JS, Gogos AJ, Pereira MP, Morshed RA, Li J, Barkovich MJ, Hervey-Jumper SL, Berger MS (2021) Effects of ventricular entry on patient outcome during glioblastoma resection. J Neurosurg. https://doi.org/10.3171/2020.7.Jns201362
doi: 10.3171/2020.7.Jns201362
pubmed: 34798608
Zhang K, Yang Y, Zhuang J, Guo G, Chao X, Zhang Z (2022) Intracranial dissemination of glioblastoma multiforme: a case report and literature review. J Int Med Res 50:3000605221112047. https://doi.org/10.1177/03000605221112047
doi: 10.1177/03000605221112047
pubmed: 35854630
Bae JS, Yang SH, Yoon WS, Kang SG, Hong YK, Jeun SS (2011) The clinical features of spinal leptomeningeal dissemination from malignant gliomas. J Kor Neurosurg Soc 49:334–338. https://doi.org/10.3340/jkns.2011.49.6.334
doi: 10.3340/jkns.2011.49.6.334
Cahill DP (2021) Extent of resection of glioblastoma: a critical evaluation in the molecular era. Neurosurg Clin N Am 32:23–29. https://doi.org/10.1016/j.nec.2020.09.006
doi: 10.1016/j.nec.2020.09.006
pubmed: 33223023
Revilla-Pacheco F, Rodríguez-Salgado P, Barrera-Ramírez M, Morales-Ruiz MP, Loyo-Varela M, Rubalcava-Ortega J, Herrada-Pineda T (2021) Extent of resection and survival in patients with glioblastoma multiforme: Systematic review and meta-analysis. Medicine 100:e26432. https://doi.org/10.1097/md.0000000000026432
doi: 10.1097/md.0000000000026432
pubmed: 34160432
pmcid: 8238332
John JK, Robin AM, Pabaney AH, Rammo RA, Schultz LR, Sadry NS, Lee IY (2017) Complications of ventricular entry during craniotomy for brain tumor resection. J Neurosurg 127:426–432. https://doi.org/10.3171/2016.7.Jns16340
doi: 10.3171/2016.7.Jns16340
pubmed: 27813467
Mistry AM, Kelly PD, Gallant JN, Mummareddy N, Mobley BC, Thompson RC, Chambless LB (2019) Comparative analysis of subventricular zone glioblastoma contact and ventricular entry during resection in predicting dissemination, hydrocephalus, and survival. Neurosurgery 85:E924-e932. https://doi.org/10.1093/neuros/nyz144
doi: 10.1093/neuros/nyz144
pubmed: 31058968
pmcid: 6904848
Sanai N, Tramontin AD, Quiñones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-García 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. https://doi.org/10.1038/nature02301
doi: 10.1038/nature02301
pubmed: 14973487
Sanai N, Alvarez-Buylla A, Berger MS (2005) Neural stem cells and the origin of gliomas. N Engl J Med 353:811–822. https://doi.org/10.1056/NEJMra043666
doi: 10.1056/NEJMra043666
pubmed: 16120861
Berendsen S, van Bodegraven E, Seute T, Spliet WGM, Geurts M, Hendrikse J, Schoysman L, Huiszoon WB, Varkila M, Rouss S, Bell EH, Kroonen J, Chakravarti A, Bours V, Snijders TJ, Robe PA (2019) Adverse prognosis of glioblastoma contacting the subventricular zone: biological correlates. PLoS ONE 14:e0222717. https://doi.org/10.1371/journal.pone.0222717
doi: 10.1371/journal.pone.0222717
pubmed: 31603915
pmcid: 6788733
Awad AW, Karsy M, Sanai N, Spetzler R, Zhang Y, Xu Y, Mahan MA (2017) Impact of removed tumor volume and location on patient outcome in glioblastoma. J Neurooncol 135:161–171. https://doi.org/10.1007/s11060-017-2562-1
doi: 10.1007/s11060-017-2562-1
pubmed: 28685405
Molinaro AM, Hervey-Jumper S, Morshed RA, Young J, Han SJ, Chunduru P, Zhang Y, Phillips JJ, Shai A, Lafontaine M, Crane J, Chandra A, Flanigan P, Jahangiri A, Cioffi G, Ostrom Q, Anderson JE, Badve C, Barnholtz-Sloan J, Sloan AE, Erickson BJ, Decker PA, Kosel ML, LaChance D, Eckel-Passow J, Jenkins R, Villanueva-Meyer J, Rice T, Wrensch M, Wiencke JK, Oberheim Bush NA, Taylor J, Butowski N, Prados M, Clarke J, Chang S, Chang E, Aghi M, Theodosopoulos P, McDermott M, Berger MS (2020) Association of maximal extent of resection of contrast-enhanced and non-contrast-enhanced tumor with survival within molecular subgroups of patients with newly diagnosed glioblastoma. JAMA Oncol 6:495–503. https://doi.org/10.1001/jamaoncol.2019.6143
doi: 10.1001/jamaoncol.2019.6143
pubmed: 32027343
pmcid: 7042822
Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, Berger MS, Parsa AT (2012) Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. J Neurosurg 117:1032–1038. https://doi.org/10.3171/2012.9.Jns12504
doi: 10.3171/2012.9.Jns12504
pubmed: 23039151
Piper RJ, Senthil KK, Yan JL, Price SJ (2018) Neuroimaging classification of progression patterns in glioblastoma: a systematic review. J Neurooncol 139:77–88. https://doi.org/10.1007/s11060-018-2843-3
doi: 10.1007/s11060-018-2843-3
pubmed: 29603080
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
doi: 10.1016/j.wneu.2017.04.053
pubmed: 28434963
Weller M, van den Bent M, Preusser M, Le Rhun E, Tonn JC, Minniti G, Bendszus M, Balana C, Chinot O, Dirven L, French P, Hegi ME, Jakola AS, Platten M, Roth P, Rudà R, Short S, Smits M, Taphoorn MJB, von Deimling A, Westphal M, Soffietti R, Reifenberger G, Wick W (2021) EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol 18:170–186. https://doi.org/10.1038/s41571-020-00447-z
doi: 10.1038/s41571-020-00447-z
pubmed: 33293629
Castro BA, Imber BS, Chen R, McDermott MW, Aghi MK (2017) Ventriculoperitoneal Shunting for Glioblastoma: Risk Factors, Indications, and Efficacy. Neurosurgery 80:421–430. https://doi.org/10.1227/neu.0000000000001263
doi: 10.1227/neu.0000000000001263
pubmed: 27218235
pmcid: 6257011
Müther M, Stummer W (2020) Ependymal fluorescence in fluorescence-guided resection of malignant glioma: a systematic review. Acta Neurochir 162:365–372. https://doi.org/10.1007/s00701-019-04144-4
doi: 10.1007/s00701-019-04144-4
pubmed: 31754847
Vertosick FT, Jr, Selker RG (1990) Brain stem and spinal metastases of supratentorial glioblastoma multiforme: a clinical series. Neurosurgery 27:516–521; discussion 521–512. https://doi.org/10.1097/00006123-199010000-00002
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 Oncol 12:233–242. https://doi.org/10.1093/neuonc/nop027
doi: 10.1093/neuonc/nop027
pubmed: 20167811
pmcid: 2940588
Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D, Isachenko N, Fouse SD, Phillips JJ, Cheresh DA, Park M, Bergers G (2012) VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 22:21–35. https://doi.org/10.1016/j.ccr.2012.05.037
doi: 10.1016/j.ccr.2012.05.037
pubmed: 22789536
pmcid: 4068350
Marquardt G, Setzer M, Lang J, Seifert V (2002) Delayed hydrocephalus after resection of supratentorial malignant gliomas. Acta Neurochir 144: 227–231; discussion 231. https://doi.org/10.1007/s007010200030
Mistry AM, Hale AT, Chambless LB, Weaver KD, Thompson RC, Ihrie RA (2017) Influence of glioblastoma contact with the lateral ventricle on survival: a meta-analysis. J Neurooncol 131:125–133. https://doi.org/10.1007/s11060-016-2278-7
doi: 10.1007/s11060-016-2278-7
pubmed: 27644688
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. https://doi.org/10.1016/j.jocn.2013.02.007
doi: 10.1016/j.jocn.2013.02.007
pubmed: 23928040
pmcid: 4086640
Comas S, Luguera E, Molero J, Balaña C, Estival A, Castañer S, Carrato C, Hostalot C, Teixidor P, Villà S (2021) Influence of glioblastoma contact with the subventricular zone on survival and recurrence patterns. Clin Transl Oncol 23:554–564. https://doi.org/10.1007/s12094-020-02448-x
doi: 10.1007/s12094-020-02448-x
pubmed: 32728970
Yang W, Xu T, Garzon-Muvdi T, Jiang C, Huang J, Chaichana KL (2018) Survival of ventricular and periventricular high-grade gliomas: a surveillance, epidemiology, and end results program-based study. World Neurosurg 111:e323–e334. https://doi.org/10.1016/j.wneu.2017.12.052
doi: 10.1016/j.wneu.2017.12.052
pubmed: 29258929
Chaichana K, Parker S, Olivi A, Quiñones-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. https://doi.org/10.3171/2009.9.Jns09805
doi: 10.3171/2009.9.Jns09805
pubmed: 19817542
Tselikas L, Souillard-Scemama R, Naggara O, Mellerio C, Varlet P, Dezamis E, Domont J, Dhermain F, Devaux B, Chrétien F, Meder JF, Pallud J, Oppenheim C (2015) Imaging of gliomas at 1.5 and 3 Tesla - A comparative study. Neuro Oncol 17:895–900. https://doi.org/10.1093/neuonc/nou332
doi: 10.1093/neuonc/nou332
pubmed: 25526734
Zikou A, Sioka C, Alexiou GA, Fotopoulos A, Voulgaris S, Argyropoulou MI (2018) Radiation necrosis, pseudoprogression, pseudoresponse, and tumor recurrence: imaging challenges for the evaluation of treated gliomas. Contrast Media Mol Imaging 2018:6828396. https://doi.org/10.1155/2018/6828396
doi: 10.1155/2018/6828396
pubmed: 30627060
pmcid: 6305027
Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8. https://doi.org/10.3171/2011.2.jns10998
doi: 10.3171/2011.2.jns10998
pubmed: 21417701
Wykes V, Zisakis A, Irimia M, Ughratdar I, Sawlani V, Watts C (2021) Importance and evidence of extent of resection in glioblastoma. J Neurol Surg Part A 82:75–86. https://doi.org/10.1055/s-0040-1701635
doi: 10.1055/s-0040-1701635
Li YM, Suki D, Hess K, Sawaya R (2016) The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection? J Neurosurg 124:977–988. https://doi.org/10.3171/2015.5.Jns142087
doi: 10.3171/2015.5.Jns142087
pubmed: 26495941
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. https://doi.org/10.3171/jns.2005.102.4.0622
doi: 10.3171/jns.2005.102.4.0622
pubmed: 15871503
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. https://doi.org/10.4103/2152-7806.68337
doi: 10.4103/2152-7806.68337
pubmed: 20847921
pmcid: 2940100