The impact of intra-operative magnetic resonance imaging and 5-ALA in the achievement of gross total resection of gliomas: A systematic literature review and meta-analysis.
Main Article Content
Abstract
In an effort to maximize extent of resection (EOR) regarding gliomas, intraoperative MRI (i-MRI) and 5-aminolevulinic acid (5-ALA) have been developed. Our study aimed to investigate the comparative contribution of 5-aminolevulinic acid and i-MRI in maximizing EOR in gliomas.
We searched the PubMed and ScienceDirect services for randomized controlled trials, controlled trials and interrupted time series studies evaluating the effect of i-MRI on gross total resection (GTR) rates and on overall survival in glioma patients. Our primary study endpoint was the definition of the percentage of patients who were offered GTR. Other relevant points of interest included the determination of overall and progression-free survival and subgroup analyses for level of evidence.
I-MRI aids in achieving GTR (odds ratio 2.71, p<0.0001). Magnet field strength does not affect significantly either GTR rates (p=0.08). The cost of the procedure is dependent on the workload of the i-MRI system. These data suggest that i-MRI or 5-ALA improves progression-free and overall survival, although there are several restrictions related to their effectiveness and reliability.
I-MRI and 5-ALA are considered to be effective adjuncts in the achievement of GTR of gliomas. When these methods are compared, there is no definite conclusion regarding which method is more effective.
Article Details
How to Cite
PANAGOPOULOS, Dimitrios et al.
The impact of intra-operative magnetic resonance imaging and 5-ALA in the achievement of gross total resection of gliomas: A systematic literature review and meta-analysis..
Medical Research Archives, [S.l.], v. 10, n. 4, apr. 2022.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2773>. Date accessed: 25 apr. 2024.
doi: https://doi.org/10.18103/mra.v10i4.2773.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, et al. The epidemiology of glioma in adults: a "state of the science" review. Neuro-oncology 2014;16(7):896-913.
2. Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. Journal of neuro-oncology 2016;130(2):269-282.
3. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008;62(4):753-764; discussion 264-756.
4. Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, et al. Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. Journal of neurosurgery 2012;117(6):1032-1038.
5. Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, et al. Association of the Extent of Resection with Survival in Glioblastoma: A Systematic Review and Meta-analysis. JAMA oncology 2016;2(11):1460-1469.
6. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. Journal of Neurosurgery 2001;95(2):190-198.
7. Mann BS. Overall survival benefit from surgical resection in treatment of recurrent glioblastoma. Annals of oncology: official journal of the European Society for Medical Oncology 2014;25(9):1866-1867.
8. Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN. Prognostic Implications of Extent of Resection in Glioblastoma: Analysis from a Large Database. World Neurosurgery 2017;(103):330-340.
9. Eljamel MS, Hofer M. From letterbox to keyhole approach for resecting intracranial lesions. Stereotactic and functional neurosurgery 2003;81(1-4):30-36.
10. Mahboob S, McPhillips R, Qiu Z, Jiang Y, Meggs C, Schiavone G, et al. Intraoperative Ultrasound-Guided Resection of Gliomas: A Meta-Analysis and Review of the Literature. World Neurosurgery 2016;(92):255-263.
11. Golub D, Hyde J, Dogra S, Nicholson J, Kirkwood K.A, Gohel P, Loftus S, H Schwartz T.H. Intraoperative MRI versus 5-ALA in high-grade glioma resection: a network meta-analysis. J Neurosurg 2020;(21);1-15.
12. Otrom QT, Gittleman H, Liao P, Vecchione-Koval T, Wolinsky Y, Kruchko C, et al: CBTRUS Statistical Report: primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol 2017;(19) (suppl_5): v1–v88.
13. Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, et al. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 2015;(372):2481–2498.
14. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 2008;(63):700–708.
15. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 2011;(115):3–8.
16. Yang K, Nath S, Koziarz A, Badhiwala JH, Ghayur H, Sourour M, et al. Biopsy versus subtotal versus gross total resection in patients with low-grade glioma: a systematic review and meta-analysis. World Neurosurg 2018;(120):e762–e775.
17. Gerard IJ, Kersten-Oertel M, Petrecca K, Sirhan D, Hall JA, Collins DL. Brain shift in neuronavigation of brain tumors: a review. Med Image Anal 2017;(35):403–420.
18. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, et al. Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 1998;(42):518–526.
19. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006;(7):392– 401.
20. Zhao S, Wu J, Wang C, Liu H, Dong X, Shi C, et al. Intraoperative fluorescence-guided resection of high-grade malignant gliomas using 5-aminolevulinic acid-induced porphyrins: a systematic review and meta-analysis of prospective studies. PLoS One 2013;(8): e63682.
21. Tronnier VM, Wirtz CR, Knauth M, Lenz G, Pastyr O, Bonsanto MM, et al. Intraoperative diagnostic and interventional magnetic resonance imaging in neurosurgery. Neurosurgery 1997;(40):891–902.
22. Kubben PL, Scholtes F, Schijns OE, Ter Laak-Poort MP, Teernstra OP, Kessels AG, et al. Intraoperative magnetic resonance imaging versus standard neuronavigation for the neurosurgical treatment of glioblastoma: a randomized controlled trial. Surg Neurol Int 2014;(5):70.
23. Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011;(12):997–1003.
24. Mislow JM, Golby AJ, Black PM. Origins of intraoperative MRI. Neurosurgery Clinics of North America 2009;20(2):137-146.
25. Nimsky C, Ganslandt O, Fahlbusch R. 1.5 T intraoperative imaging beyond standard anatomic imaging. Neurosurgery Clinics of North America 2005;16(1):185-200, vii.
26. Liang D, Schulder M. The role of intraoperative magnetic resonance imaging in glioma surgery. Surgical neurology international 2012;(3) (Suppl 4): S320-327.
27. Price SJ, Gillard JH. Imaging biomarkers of brain tumour margin and tumour invasion. The British journal of radiology 2011;(84) Spec No 2:S159-167.
28. Dadario N.B, Khatri D, Reichman N, Nwagwu C.D, D'Amico R.S. 5-Aminolevulinic Acid-Shedding Light on Where to Focus. World Neurosurg 2021;(150):9-16. doi: 10.1016/j.wneu.2021.02.118.
29. Mansouri A, Mansouri S, Hachem LD, et al. The role of 5-aminolevulinic acid in enhancing surgery for high-grade glioma, its current boundaries, and future perspectives: a systematic review. Cancer 2016;(122):2469-2478.
30. Coburger J, Scheuerle A, Pala A, Thal D, Wirtz CR, König R. Histopathological insights on imaging results of intraoperative magnetic resonance imaging, 5-aminolevulinic acid, and intraoperative ultrasound in glioblastoma surgery. Neurosurgery 2017;(81):165–174.
31. Eyüpoglu IY, Hore N, Merkel A, Buslei R, Buchfelder M, Savaskan N. Supra-complete surgery via dual intraoperative visualization approach (DiVA) prolongs patient survival in glioblastoma. Oncotarget 2016;(7):25755–25768.
32. Eyüpoglu IY, Hore N, Savaskan NE, Grummich P, Roessler K, Buchfelder M, et al. Improving the extent of malignant glioma resection by dual intraoperative visualization approach. PLoS One 2012;(7): e44885.
33. Gessler F, Forster MT, Duetzmann S, Mittelbronn M, Hattingen E, Franz K, et al. Combination of intraoperative magnetic resonance imaging and intraoperative fluorescence to enhance the resection of contrast enhancing gliomas. Neurosurgery 2015;(77):16–22.
34. Hauser SB, Kockro RA, Actor B, Sarnthein J, Bernays RL. Combining 5-aminolevulinic acid fluorescence and intraoperative magnetic resonance imaging in glioblastoma surgery: a histology-based evaluation. Neurosurgery 2016;(78):475–483.
35. Nickel K, Renovanz M, König J, Stöckelmaier L, Hickmann AK, Nadji-Ohl M, et al. The patients’ view: impact of the extent of resection, intraoperative imaging, and awake surgery on health-related quality of life in high-grade glioma patients—results of a multicenter cross-sectional study. Neurosurg Rev 2018;(41):207–219.
36. Quick-Weller J, Lescher S, Forster MT, Konczalla J, Seifert V, Senft C. Combination of 5-ALA and i-MRI in re-resection of recurrent glioblastoma. Br J Neurosurg 2016;(30):313–317.
37. Schatlo B, Fandino J, Smoll NR, Wetzel O, Remonda L, Marbacher S, et al. Outcomes after combined use of intraoperative MRI and 5-aminolevulinic acid in high-grade glioma surgery. Neuro Oncol 2015;(17):1560–1567.
38. Tsugu A, Ishizaka H, Mizokami Y, Osada T, Baba T, Yoshiyama M, et al. Impact of the combination of 5-aminolevulinic acid-induced fluorescence with intraoperative magnetic resonance imaging-guided surgery for glioma. World Neurosurg 2011;(76):120–127.
39. Yamada S, Muragaki Y, Maruyama T, Komori T, Okada Y. Role of neurochemical navigation with 5-aminolevulinic acid during intraoperative MRI-guided resection of intracranial malignant gliomas. Clin Neurol Neurosurg 2015;(130):134–139.
40. Chen LF, Yang Y, Ma XD, Yu XG, Gui QP, Xu BN, et al. Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 2017;(27):696–706.
41. Napolitano M, Vaz G, Lawson TM, Docquier MA, van Maanen A, Duprez T, et al. Glioblastoma surgery with and without intraoperative MRI at 3.0T. Neurochirurgie 2014;(60):143–150.
42. Roder C, Bisdas S, Ebner FH, Honegger J, Naegele T, Ernemann U, et al. Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol 2014;(40):297–304.
43. Senft C, Franz K, Blasel S, Oszvald A, Rathert J, Seifert V, et al. Influence of iMRI-guidance on the extent of resection and survival of patients with glioblastoma multiforme. Technol Cancer Res Treat 2010;(9):339–346.
44. Wu JS, Gong X, Song YY, Zhuang DX, Yao CJ, Qiu TM, et al. 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 2014;(61) (Suppl 1):145–154.
45. Zhang J, Chen X, Zhao Y, Wang F, Li F, Xu B. Impact of intraoperative magnetic resonance imaging and functional neuronavigation on surgical outcome in patients with gliomas involving language areas. Neurosurg Rev 2015;(38):319–330.
46. Barbosa BJ, Mariano ED, Batista CM, Marie SK, Teixeira MJ, Pereira CU, et al. Intraoperative assistive technologies and extent of resection in glioma surgery: a systematic review of prospective controlled studies. Neurosurg Rev 2015;(38):217–227.
47. Stummer W, Tonn JC, Mehdorn HM, Nestler U, Franz K, Goetz C, et al. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. J Neurosurg 2011;(114):613–623.
48. Bruch JD, Ho J, Watts C, Price SJ. A single centre case control study of the efficacy and safety of 5-aminolevulinic acid guided resections of grade IV (WHO) glioblastomas. Neuro Oncol 2011;(13) (Suppl 2): ii1–ii14.
49. Díez Valle R, Slof J, Galván J, Arza C, Romariz C, Vidal C. Observational, retrospective study of the effectiveness of 5-aminolevulinic acid in malignant glioma surgery in Spain (The VISIONA study). Neurologia 2014;(29):131–138.
50. Kim SK, Choi SH, Kim YH, Park CK. Impact of fluorescence-guided surgery on the improvement of clinical outcomes in glioblastoma patients. Neurooncol Pract 2014;(1):81–85.
51. Knauth M, Wirtz CR, Tronnier VM, Aras N, Kunze S, Sartor K. Intraoperative MR imaging increases the extent of tumor resection in patients with high-grade gliomas. AJNR American journal of neuroradiology 1999;20(9):1642-1646.
52. Mehdorn HM, Schwarz F, Dawirs S, Hedderich J, Doerner L, Nabavi A. High-Field i-MRI in Glioblastoma Surgery: Improvement of Resection Radicality and Survival for the Patient? Pamir MN, Seifert V, Kiris T, editors: Springer Wien New York; 2011.
53. Napolitano M, Vaz G, Lawson TM, Docquier MA, van Maanen A, Duprez T, et al. Glioblastoma surgery with and without intraoperative MRI at 3.0T. Neuro-Chirurgie 2014;60(4):143-150.
54. Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R. Intraoperative visualization for resection of gliomas: the role of functional neuronavigation and intraoperative 1.5 T MRI. Neurological research 2006;28(5):482-487.
55. Olubiyi OI, Ozdemir A, Incekara F, Tie Y, Dolati P, Hsu L, et al. Intraoperative Magnetic Resonance Imaging in Intracranial Glioma Resection: A Single-Center, Retrospective Blinded Volumetric Study. World neurosurgery 2015;84(2):528-536.
56. Caras A, Mugge L, Miller W.K, Mansour T.R, Schroeder J, Medhkou A. Usefulness and Impact of Intraoperative Imaging for Glioma Resection on Patient Outcome and Extent of Resection: A Systematic Review and Meta-Analysis. World Neurosurg 2020;(134):98-110.
57. Yahanda A.T, Patel B, Sutherland G, Honeycutt J, Jensen R.L, Smyth M.D, et. al. A Multi-Institutional Analysis of Factors Influencing Surgical Outcomes for Patients with Newly Diagnosed Grade I Gliomas. World Neurosurg 2020;(135): e754-e764.
58. Choudhri XAF, Klimo P, Auschwitz TS, Whitehead MT, Boop FA. 3T intraoperative MRI for management of pediatric CNS neoplasms. Am J Neuroradiol 2014;(35):2382-2387.
59. Haydon DH, Chicoine MR, Dacey RG Jr. The impact of high-field-strength intraoperative magnetic resonance imaging on brain tumor management. Clin Neurosurg 2013;(60) (suppl.1):92-9.
60. Kremer P, Tronnier V, Steiner HH, et al. Intraoperative MRI for interventional neurosurgical procedures and tumor resection control in children. Childs Nerv Syst. 2006;(22):674-678.
61. Roder C, Breitkopf MS, Bisdas S, et al. Beneficial impact of high-field intraoperative magnetic resonance imaging on the efficacy of pediatric low-grade glioma surgery. Neurosurg Focus. 2016;(40): E13.
62. Haydon DH, Dahiya S, Smyth MD, Limbrick DD, Leonard JR. Greater extent of resection improves ganglioglioma recurrence-free survival in children: a volumetric analysis. Neurosurgery. 2014;(75):37-42.
63. Forsyth PA, Shaw EG, Scheithauer BW,O’Fallon JR, Layton DD, Katzmann JA. Supratentorial pilocytic astrocytomas. A clinicopathologic, prognostic, and flow cytometric study of 51 patients. Cancer. 1993;(72):1335-1342.
64. Stüer C, Vilz B, Majores M, Becker A, Schramm J, Simon M. Frequent recurrence and progression in pilocytic astrocytoma in adults. Cancer 2007;(110):2799-2808.
65. Leroy H-A, Delmaire C, Le Rhun E, Drumez E, Lejeune J-P, Reyns N. High-field intraoperative MRI and glioma surgery: results after the first 100 consecutive patients. Acta Neurochir (Wien) 2019;161(7):1467-1474.
66. Feigl G.C, Heckl S, Kullmann M, Filip Z, Decker K, Klein J, Ernemann U, Tatagiba M, Velnar T, Ritz R. Review of first clinical experiences with a 1.5 Tesla ceiling-mounted moveable intraoperative MRI system in Europe. Bosn J Basic Med Sci. 2019;19(1):24–30.
67. Pichierri A, Bradley M, Iyer V. Intraoperative Magnetic Resonance Imaging-Guided Glioma Resections in Awake or Asleep Settings and Feasibility in the Context of a Public Health System. World Neurosurg X 2019;(20); 3:100022.
68. Krivosheya D, Rao G, Tummala S, Kumar V, Suki D, Bastos D.C.A, Sujit S, Prabhu S. Impact of Multi-modality Monitoring Using Direct Electrical Stimulation to Determine Corticospinal Tract Shift and Integrity in Tumors using the Intraoperative MRI. J Neurol Surg A Cent Eur Neurosurg 2021;82(4):375-380.
69. Wach J, Goetz C, Shareghi K, Scholz T, Heßelmann V, Mager A-K, Gottschalk J, Vatter H, Paul Kremer P. Dual-Use Intraoperative MRI in Glioblastoma Surgery: Results of Resection, Histopathologic Assessment, and Surgical Site Infections. J Neurol Surg A Cent Eur Neurosurg 2019;80(6):413-422.
70. D’Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of resection in glioma-a review of the cutting edge. World Neurosurg. 2017;(103):538-549.
71. Khatri D, Das K, Gosal J, et al. Surgery in high-grade insular tumors: oncological and seizure outcomes from 41 consecutive patients. Asian J Neurosurg 2020;(15):537-544.
72. Khatri D, Jaiswal A, Das KK, Pandey S, Bhaisora K, Kumar R. Health-related quality of life after surgery in supratentorial gliomas. Neurol India. 2019;(67):467-475.
73. Patel NV, Khatri D, D’Amico R, et al. Vascularized temporoparietal fascial flap: a novel surgical technique to bypass the blood-brain barrier in glioblastoma. World Neurosurg 2020;(143):38-45.
74. Chow DS, Khatri D, Chang PD, Zlochower A, Boockvar JA, Filippi CG. Updates on deep learning and glioma: use of convolutional neural networks to image glioma heterogeneity. Neuroimaging Clin North Am 2020;(30):493-503.
75. Abrams M, Reichman N, Khatri D, et al. Update on glioma biotechnology. Clin Neurol Neurosurg 2020;(195):106075.
76. Zlochower A, Chow DS, Chang P, Khatri D, Boockvar JA, Filippi CG. Deep learning AI applications in the imaging of glioma. Top Magn Reson Imaging 2020;(29):115.
77. D’Amico RS, Khatri D, Reichman N, et al. Super selective intra-arterial cerebral infusion of modern chemotherapeutics after blood-brain barrier disruption: where are we now, and where we are going. J Neurooncol 2020;(147):261-278.
78. Hadjipanayis CG, Widhalm G, Stummer W. What is the surgical benefit of utilizing 5-aminolevulinic acid for fluorescence-guided surgery of malignant gliomas? Neurosurgery 2015;(77):663-673.
79. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 2000;(93):1003-1013.
80. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomized controlled multicentre phase III trial. Lancet Oncol 2006;(7):392-401.
81. Gandhi S, Tayebi Meybodi A, Belykh E, et al. Survival outcomes among patients with high-grade glioma treated with 5-aminolevulinic acide guided surgery: a systematic review and meta-analysis. Front Oncol 2019;(9):620.
82. Schucht P, Knittel S, Slotboom J, et al. 5-ALA complete resections go beyond MR contrast enhancement: shift corrected volumetric analysis of the extent of resection in surgery for glioblastoma. Acta Neurochir (Wien) 2014;(156):305-312.
83. Stummer W, Tonn J-C, Goetz C, et al. 5-Aminolevulinic acid-derived tumor fluorescence: the diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and postoperative imaging. Neurosurgery 2014;(74):310-320.
84. Richter JCO, Haj-Hosseini N, Hallbeck M, Wårdell K. Combination of hand-held probe and microscopy for fluorescence guided surgery in the brain tumor marginal zone. Photodiagnosis Photodyn Ther 2017;(18):185-192.
85. Widhalm G, Kiesel B, Woehrer A, et al. 5-aminolevulinic acid induced fluorescence is a powerful intraoperative marker for precise histopathological grading of gliomas with non-significant contrast-enhancement. PLoS One 2013;(8): e76988.
86. Jaber M, Wölfer J, Ewelt C, et al. The value of 5-aminolevulinic acid in low-grade gliomas and high-grade gliomas lacking glioblastoma imaging features: an analysis based on fluorescence, magnetic resonance imaging, 18f-fluoroethyltyrosine positron emission tomography, and tumor molecular factors. Neurosurgery 2016;(78):401-411.
87. Smith EJ, Gohil K, Thompson CM, Naik A, Hassaneen W. Fluorescein-Guided Resection of High-Grade Gliomas: A Meta-Analysis. World Neurosurg 2021;(4): S1878-8750(21)01314-0.
88. La Rocca G, Sabatino G, Menna G, Altieri R, Ius T, Marchese E, Olivi A, Barresi V, Della Pepa G.M. 5-Aminolevulinic Acid False Positives in Cerebral Neuro-Oncology: Not All That Is Fluorescent Is Tumor. A Case-Based Update and Literature Review. World Neurosurg 2020;(137):187-193.
89. Nestler U, Warter A, Cabre P, Manzo N. A case of late-onset multiple sclerosis mimicking glioblastoma and displaying intraoperative 5-aminolevulinic acid fluorescence. Acta Neurochir (Wien) 2012;(154):899-901.
90. Miyatake S, Kuroiwa T, Kajimoto Y, Miyashita M, Tanaka H, Tsuji M. Fluorescence of non-neoplastic, magnetic resonance imaging enhancing tissue by 5-aminolevulinic acid: case report. Neurosurgery 2007;(61):E1101-E1103 [discussion: E1103-110].
91. Voellger B, Klein J, Mawrin C, Firsching R. 5-Aminolevulinic acid (5-ALA) fluorescence in infectious disease of the brain. Acta Neurochir (Wien) 2014; (156):1977-1978.
92. Solis WG, Hansen M. Fluorescence in a cryptococcoma following administration of 5-aminolevulinic acid hydrochloride (Gliolan). BMJ Case Rep 2017;(11);2017: bcr2017219469.
93. Omoto K, Matsuda R, Nakagawa I, Motoyama Y, Nakase H. False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: a case-report. Surg Neurol Int 2018;(9):49.
94. de Laurentis C, Del Bene M, Fociani P, Tonello C, Pollo B, DiMeco F. 5-ALA fluorescence in case of brain abscess by Aggregatibacter mimicking glioblastoma. World Neurosurg 2019;(125):175-1.
95. Picart T, Berhouma M, Dumot C, Pallud J, Metellus P, Armoiry X, Guyotat J. Optimization of high-grade glioma resection using 5-ALA fluorescence-guided surgery: A literature review and practical recommendations from the neuro-oncology club of the French society of neurosurgery. Neurochirurgie 2019;65(4):164-177.
96. Valle R.D, Hadjipanayis C.G, Stummer W. Established and emerging uses of 5-ALA in the brain: an overview. Neurooncol 2019;141(3):487-494.
97. Stepp H, Stummer W. 5-ALA in the management of malignant glioma. Lasers Surg Med 2018;50(5):399-419.
98. Hollon T, Stummer W, Orringer D, Molina E.S. Surgical Adjuncts to Increase the Extent of Resection: Intraoperative MRI, Fluorescence, and Raman Histology. Neurosurg Clin N Am 2019;30(1):65-74.
99. Kamp M.A, Molle Z.K, Munoz-Bendix C, Rapp M, Sabel M, Steiger H-J, Cornelius J.F. Various shades of red-a systematic analysis of qualitative estimation of ALA-derived fluorescence in neurosurgery. Neurosurg Rev 2018;41(1):3-18.
100. Leuthardt EC, Lim CCH, Shah MN, et al. Use of movable high-field-strength intraoperative magnetic resonance imaging with awake craniotomies for resection of gliomas: preliminary experience. Neurosurgery 2011;(69):194-205.
101. Li P, Qian R, Niu C, Fu X. Impact of intraoperative MRI-guided resection on resection and survival in patient with gliomas: a meta-analysis. Current medical research and opinion 2017;33(4):621-630.
102. Marongiu A, D'Andrea G, Raco A. 1.5-T Field Intraoperative Magnetic Resonance Imaging Improves Extent of Resection and Survival in Glioblastoma Removal. World neurosurgery 2017;(98):578-586.
103. Coburger J, Segovia von Riehm J, Ganslandt O, Wirtz CR, Renovanz M. Is There an Indication for Intraoperative MRI in Subtotal Resection of Glioblastoma? A Multicenter Retrospective Comparative Analysis. World neurosurgery 2018;(110): e389-e397.
104. Familiari P, Frati A, Pesce A, Miscusi M, Cimatti M, Raco A. Real Impact of Intraoperative Magnetic Resonance Imaging in Newly Diagnosed Glioblastoma Multiforme Resection: An Observational Analytic Cohort Study from a Single Surgeon Experience. World neurosurgery 2018;(116): e9-e17.
105. Makary M, Chiocca EA, Erminy N, Antor M, Bergese SD, Abdel-Rasoul M, et al. Clinical and economic outcomes of low-field intraoperative MRI-guided tumor resection neurosurgery. Journal of magnetic resonance imaging: JMRI 2011;34(5):1022-1030.
106. Ranganathan P, Pramesh CS, Aggarwal R. Common pitfalls in statistical analysis: Absolute risk reduction, relative risk reduction, and number needed to treat. Perspectives in clinical research 2016;7(1):51-53.
107. Gousias K, Markou M, Voulgaris S, Goussia A, Voulgari P, Bai M, et al. Descriptive epidemiology of cerebral gliomas in northwest Greece and study of potential predisposing factors, 2005-2007. Neuroepidemiology 2009;33(2):89-95.
108. Uyl-de Groot CA, Stupp R, van der Bent M. Cost-effectiveness of temozolomide for the treatment of newly diagnosed glioblastoma multiforme. Expert review of pharmaco-economics & outcomes research 2009;9(3):235-241.
109. Martikainen JA, Kivioja A, Hallinen T, Vihinen P. Economic evaluation of temozolomide in the treatment of recurrent glioblastoma multiforme. Pharmaco Economics 2005;23(8):803-815.
110. Garside R, Pitt M, Anderson R, Rogers G, Dyer M, Mealing S, et al. The effectiveness and cost-effectiveness of carmustine implants and temozolomide for the treatment of newly diagnosed high-grade glioma: a systematic review and economic evaluation. Health technology assessment 2007;11(45): iii-iv, ix-221.
111. Messali A, Hay JW, Villacorta R. The cost-effectiveness of temozolomide in the adjuvant treatment of newly diagnosed glioblastoma in the United States. Neuro-oncology 2013;15(11):1532-1542.
112. Brauer CA, Rosen AB, Olchanski NV, Neumann PJ. Cost-utility analyses in orthopaedic surgery. The Journal of bone and joint surgery American volume 2005;87(6):1253-1259.
113. Sachs JD, Ahluwalia IJ, K.Y. A, E. A, D. C, Z. D, et al. Macroeconomics and Health: Investing in Health for Economic Development. November 2001.
114. Li Y, Ali S, Clarke J, Cha S. Bevacizumab in Recurrent Glioma: Patterns of Treatment Failure and Implications. Brain tumor research and treatment 2017;5(1):1-9.
115. Kovic B, Xie F. Economic Evaluation of Bevacizumab for the First-Line Treatment of Newly Diagnosed Glioblastoma Multiforme. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2015;33(20):2296-2302.
116. Eljamel MS, Mahboob SO. The effectiveness and cost-effectiveness of intraoperative imaging in high-grade glioma resection; a comparative review of intraoperative ALA, fluorescein, ultrasound and MRI. Photodiagnosis and photodynamic therapy 2016;(16):35-43.
117. Enchev Y. Neuronavigation: geneology, reality, and prospects. Neurosurg Focus. 2009;(27): E11.
2. Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. Journal of neuro-oncology 2016;130(2):269-282.
3. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008;62(4):753-764; discussion 264-756.
4. Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, et al. Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. Journal of neurosurgery 2012;117(6):1032-1038.
5. Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, et al. Association of the Extent of Resection with Survival in Glioblastoma: A Systematic Review and Meta-analysis. JAMA oncology 2016;2(11):1460-1469.
6. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. Journal of Neurosurgery 2001;95(2):190-198.
7. Mann BS. Overall survival benefit from surgical resection in treatment of recurrent glioblastoma. Annals of oncology: official journal of the European Society for Medical Oncology 2014;25(9):1866-1867.
8. Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN. Prognostic Implications of Extent of Resection in Glioblastoma: Analysis from a Large Database. World Neurosurgery 2017;(103):330-340.
9. Eljamel MS, Hofer M. From letterbox to keyhole approach for resecting intracranial lesions. Stereotactic and functional neurosurgery 2003;81(1-4):30-36.
10. Mahboob S, McPhillips R, Qiu Z, Jiang Y, Meggs C, Schiavone G, et al. Intraoperative Ultrasound-Guided Resection of Gliomas: A Meta-Analysis and Review of the Literature. World Neurosurgery 2016;(92):255-263.
11. Golub D, Hyde J, Dogra S, Nicholson J, Kirkwood K.A, Gohel P, Loftus S, H Schwartz T.H. Intraoperative MRI versus 5-ALA in high-grade glioma resection: a network meta-analysis. J Neurosurg 2020;(21);1-15.
12. Otrom QT, Gittleman H, Liao P, Vecchione-Koval T, Wolinsky Y, Kruchko C, et al: CBTRUS Statistical Report: primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol 2017;(19) (suppl_5): v1–v88.
13. Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, et al. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 2015;(372):2481–2498.
14. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 2008;(63):700–708.
15. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 2011;(115):3–8.
16. Yang K, Nath S, Koziarz A, Badhiwala JH, Ghayur H, Sourour M, et al. Biopsy versus subtotal versus gross total resection in patients with low-grade glioma: a systematic review and meta-analysis. World Neurosurg 2018;(120):e762–e775.
17. Gerard IJ, Kersten-Oertel M, Petrecca K, Sirhan D, Hall JA, Collins DL. Brain shift in neuronavigation of brain tumors: a review. Med Image Anal 2017;(35):403–420.
18. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, et al. Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 1998;(42):518–526.
19. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006;(7):392– 401.
20. Zhao S, Wu J, Wang C, Liu H, Dong X, Shi C, et al. Intraoperative fluorescence-guided resection of high-grade malignant gliomas using 5-aminolevulinic acid-induced porphyrins: a systematic review and meta-analysis of prospective studies. PLoS One 2013;(8): e63682.
21. Tronnier VM, Wirtz CR, Knauth M, Lenz G, Pastyr O, Bonsanto MM, et al. Intraoperative diagnostic and interventional magnetic resonance imaging in neurosurgery. Neurosurgery 1997;(40):891–902.
22. Kubben PL, Scholtes F, Schijns OE, Ter Laak-Poort MP, Teernstra OP, Kessels AG, et al. Intraoperative magnetic resonance imaging versus standard neuronavigation for the neurosurgical treatment of glioblastoma: a randomized controlled trial. Surg Neurol Int 2014;(5):70.
23. Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011;(12):997–1003.
24. Mislow JM, Golby AJ, Black PM. Origins of intraoperative MRI. Neurosurgery Clinics of North America 2009;20(2):137-146.
25. Nimsky C, Ganslandt O, Fahlbusch R. 1.5 T intraoperative imaging beyond standard anatomic imaging. Neurosurgery Clinics of North America 2005;16(1):185-200, vii.
26. Liang D, Schulder M. The role of intraoperative magnetic resonance imaging in glioma surgery. Surgical neurology international 2012;(3) (Suppl 4): S320-327.
27. Price SJ, Gillard JH. Imaging biomarkers of brain tumour margin and tumour invasion. The British journal of radiology 2011;(84) Spec No 2:S159-167.
28. Dadario N.B, Khatri D, Reichman N, Nwagwu C.D, D'Amico R.S. 5-Aminolevulinic Acid-Shedding Light on Where to Focus. World Neurosurg 2021;(150):9-16. doi: 10.1016/j.wneu.2021.02.118.
29. Mansouri A, Mansouri S, Hachem LD, et al. The role of 5-aminolevulinic acid in enhancing surgery for high-grade glioma, its current boundaries, and future perspectives: a systematic review. Cancer 2016;(122):2469-2478.
30. Coburger J, Scheuerle A, Pala A, Thal D, Wirtz CR, König R. Histopathological insights on imaging results of intraoperative magnetic resonance imaging, 5-aminolevulinic acid, and intraoperative ultrasound in glioblastoma surgery. Neurosurgery 2017;(81):165–174.
31. Eyüpoglu IY, Hore N, Merkel A, Buslei R, Buchfelder M, Savaskan N. Supra-complete surgery via dual intraoperative visualization approach (DiVA) prolongs patient survival in glioblastoma. Oncotarget 2016;(7):25755–25768.
32. Eyüpoglu IY, Hore N, Savaskan NE, Grummich P, Roessler K, Buchfelder M, et al. Improving the extent of malignant glioma resection by dual intraoperative visualization approach. PLoS One 2012;(7): e44885.
33. Gessler F, Forster MT, Duetzmann S, Mittelbronn M, Hattingen E, Franz K, et al. Combination of intraoperative magnetic resonance imaging and intraoperative fluorescence to enhance the resection of contrast enhancing gliomas. Neurosurgery 2015;(77):16–22.
34. Hauser SB, Kockro RA, Actor B, Sarnthein J, Bernays RL. Combining 5-aminolevulinic acid fluorescence and intraoperative magnetic resonance imaging in glioblastoma surgery: a histology-based evaluation. Neurosurgery 2016;(78):475–483.
35. Nickel K, Renovanz M, König J, Stöckelmaier L, Hickmann AK, Nadji-Ohl M, et al. The patients’ view: impact of the extent of resection, intraoperative imaging, and awake surgery on health-related quality of life in high-grade glioma patients—results of a multicenter cross-sectional study. Neurosurg Rev 2018;(41):207–219.
36. Quick-Weller J, Lescher S, Forster MT, Konczalla J, Seifert V, Senft C. Combination of 5-ALA and i-MRI in re-resection of recurrent glioblastoma. Br J Neurosurg 2016;(30):313–317.
37. Schatlo B, Fandino J, Smoll NR, Wetzel O, Remonda L, Marbacher S, et al. Outcomes after combined use of intraoperative MRI and 5-aminolevulinic acid in high-grade glioma surgery. Neuro Oncol 2015;(17):1560–1567.
38. Tsugu A, Ishizaka H, Mizokami Y, Osada T, Baba T, Yoshiyama M, et al. Impact of the combination of 5-aminolevulinic acid-induced fluorescence with intraoperative magnetic resonance imaging-guided surgery for glioma. World Neurosurg 2011;(76):120–127.
39. Yamada S, Muragaki Y, Maruyama T, Komori T, Okada Y. Role of neurochemical navigation with 5-aminolevulinic acid during intraoperative MRI-guided resection of intracranial malignant gliomas. Clin Neurol Neurosurg 2015;(130):134–139.
40. Chen LF, Yang Y, Ma XD, Yu XG, Gui QP, Xu BN, et al. Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 2017;(27):696–706.
41. Napolitano M, Vaz G, Lawson TM, Docquier MA, van Maanen A, Duprez T, et al. Glioblastoma surgery with and without intraoperative MRI at 3.0T. Neurochirurgie 2014;(60):143–150.
42. Roder C, Bisdas S, Ebner FH, Honegger J, Naegele T, Ernemann U, et al. Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol 2014;(40):297–304.
43. Senft C, Franz K, Blasel S, Oszvald A, Rathert J, Seifert V, et al. Influence of iMRI-guidance on the extent of resection and survival of patients with glioblastoma multiforme. Technol Cancer Res Treat 2010;(9):339–346.
44. Wu JS, Gong X, Song YY, Zhuang DX, Yao CJ, Qiu TM, et al. 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 2014;(61) (Suppl 1):145–154.
45. Zhang J, Chen X, Zhao Y, Wang F, Li F, Xu B. Impact of intraoperative magnetic resonance imaging and functional neuronavigation on surgical outcome in patients with gliomas involving language areas. Neurosurg Rev 2015;(38):319–330.
46. Barbosa BJ, Mariano ED, Batista CM, Marie SK, Teixeira MJ, Pereira CU, et al. Intraoperative assistive technologies and extent of resection in glioma surgery: a systematic review of prospective controlled studies. Neurosurg Rev 2015;(38):217–227.
47. Stummer W, Tonn JC, Mehdorn HM, Nestler U, Franz K, Goetz C, et al. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. J Neurosurg 2011;(114):613–623.
48. Bruch JD, Ho J, Watts C, Price SJ. A single centre case control study of the efficacy and safety of 5-aminolevulinic acid guided resections of grade IV (WHO) glioblastomas. Neuro Oncol 2011;(13) (Suppl 2): ii1–ii14.
49. Díez Valle R, Slof J, Galván J, Arza C, Romariz C, Vidal C. Observational, retrospective study of the effectiveness of 5-aminolevulinic acid in malignant glioma surgery in Spain (The VISIONA study). Neurologia 2014;(29):131–138.
50. Kim SK, Choi SH, Kim YH, Park CK. Impact of fluorescence-guided surgery on the improvement of clinical outcomes in glioblastoma patients. Neurooncol Pract 2014;(1):81–85.
51. Knauth M, Wirtz CR, Tronnier VM, Aras N, Kunze S, Sartor K. Intraoperative MR imaging increases the extent of tumor resection in patients with high-grade gliomas. AJNR American journal of neuroradiology 1999;20(9):1642-1646.
52. Mehdorn HM, Schwarz F, Dawirs S, Hedderich J, Doerner L, Nabavi A. High-Field i-MRI in Glioblastoma Surgery: Improvement of Resection Radicality and Survival for the Patient? Pamir MN, Seifert V, Kiris T, editors: Springer Wien New York; 2011.
53. Napolitano M, Vaz G, Lawson TM, Docquier MA, van Maanen A, Duprez T, et al. Glioblastoma surgery with and without intraoperative MRI at 3.0T. Neuro-Chirurgie 2014;60(4):143-150.
54. Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R. Intraoperative visualization for resection of gliomas: the role of functional neuronavigation and intraoperative 1.5 T MRI. Neurological research 2006;28(5):482-487.
55. Olubiyi OI, Ozdemir A, Incekara F, Tie Y, Dolati P, Hsu L, et al. Intraoperative Magnetic Resonance Imaging in Intracranial Glioma Resection: A Single-Center, Retrospective Blinded Volumetric Study. World neurosurgery 2015;84(2):528-536.
56. Caras A, Mugge L, Miller W.K, Mansour T.R, Schroeder J, Medhkou A. Usefulness and Impact of Intraoperative Imaging for Glioma Resection on Patient Outcome and Extent of Resection: A Systematic Review and Meta-Analysis. World Neurosurg 2020;(134):98-110.
57. Yahanda A.T, Patel B, Sutherland G, Honeycutt J, Jensen R.L, Smyth M.D, et. al. A Multi-Institutional Analysis of Factors Influencing Surgical Outcomes for Patients with Newly Diagnosed Grade I Gliomas. World Neurosurg 2020;(135): e754-e764.
58. Choudhri XAF, Klimo P, Auschwitz TS, Whitehead MT, Boop FA. 3T intraoperative MRI for management of pediatric CNS neoplasms. Am J Neuroradiol 2014;(35):2382-2387.
59. Haydon DH, Chicoine MR, Dacey RG Jr. The impact of high-field-strength intraoperative magnetic resonance imaging on brain tumor management. Clin Neurosurg 2013;(60) (suppl.1):92-9.
60. Kremer P, Tronnier V, Steiner HH, et al. Intraoperative MRI for interventional neurosurgical procedures and tumor resection control in children. Childs Nerv Syst. 2006;(22):674-678.
61. Roder C, Breitkopf MS, Bisdas S, et al. Beneficial impact of high-field intraoperative magnetic resonance imaging on the efficacy of pediatric low-grade glioma surgery. Neurosurg Focus. 2016;(40): E13.
62. Haydon DH, Dahiya S, Smyth MD, Limbrick DD, Leonard JR. Greater extent of resection improves ganglioglioma recurrence-free survival in children: a volumetric analysis. Neurosurgery. 2014;(75):37-42.
63. Forsyth PA, Shaw EG, Scheithauer BW,O’Fallon JR, Layton DD, Katzmann JA. Supratentorial pilocytic astrocytomas. A clinicopathologic, prognostic, and flow cytometric study of 51 patients. Cancer. 1993;(72):1335-1342.
64. Stüer C, Vilz B, Majores M, Becker A, Schramm J, Simon M. Frequent recurrence and progression in pilocytic astrocytoma in adults. Cancer 2007;(110):2799-2808.
65. Leroy H-A, Delmaire C, Le Rhun E, Drumez E, Lejeune J-P, Reyns N. High-field intraoperative MRI and glioma surgery: results after the first 100 consecutive patients. Acta Neurochir (Wien) 2019;161(7):1467-1474.
66. Feigl G.C, Heckl S, Kullmann M, Filip Z, Decker K, Klein J, Ernemann U, Tatagiba M, Velnar T, Ritz R. Review of first clinical experiences with a 1.5 Tesla ceiling-mounted moveable intraoperative MRI system in Europe. Bosn J Basic Med Sci. 2019;19(1):24–30.
67. Pichierri A, Bradley M, Iyer V. Intraoperative Magnetic Resonance Imaging-Guided Glioma Resections in Awake or Asleep Settings and Feasibility in the Context of a Public Health System. World Neurosurg X 2019;(20); 3:100022.
68. Krivosheya D, Rao G, Tummala S, Kumar V, Suki D, Bastos D.C.A, Sujit S, Prabhu S. Impact of Multi-modality Monitoring Using Direct Electrical Stimulation to Determine Corticospinal Tract Shift and Integrity in Tumors using the Intraoperative MRI. J Neurol Surg A Cent Eur Neurosurg 2021;82(4):375-380.
69. Wach J, Goetz C, Shareghi K, Scholz T, Heßelmann V, Mager A-K, Gottschalk J, Vatter H, Paul Kremer P. Dual-Use Intraoperative MRI in Glioblastoma Surgery: Results of Resection, Histopathologic Assessment, and Surgical Site Infections. J Neurol Surg A Cent Eur Neurosurg 2019;80(6):413-422.
70. D’Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of resection in glioma-a review of the cutting edge. World Neurosurg. 2017;(103):538-549.
71. Khatri D, Das K, Gosal J, et al. Surgery in high-grade insular tumors: oncological and seizure outcomes from 41 consecutive patients. Asian J Neurosurg 2020;(15):537-544.
72. Khatri D, Jaiswal A, Das KK, Pandey S, Bhaisora K, Kumar R. Health-related quality of life after surgery in supratentorial gliomas. Neurol India. 2019;(67):467-475.
73. Patel NV, Khatri D, D’Amico R, et al. Vascularized temporoparietal fascial flap: a novel surgical technique to bypass the blood-brain barrier in glioblastoma. World Neurosurg 2020;(143):38-45.
74. Chow DS, Khatri D, Chang PD, Zlochower A, Boockvar JA, Filippi CG. Updates on deep learning and glioma: use of convolutional neural networks to image glioma heterogeneity. Neuroimaging Clin North Am 2020;(30):493-503.
75. Abrams M, Reichman N, Khatri D, et al. Update on glioma biotechnology. Clin Neurol Neurosurg 2020;(195):106075.
76. Zlochower A, Chow DS, Chang P, Khatri D, Boockvar JA, Filippi CG. Deep learning AI applications in the imaging of glioma. Top Magn Reson Imaging 2020;(29):115.
77. D’Amico RS, Khatri D, Reichman N, et al. Super selective intra-arterial cerebral infusion of modern chemotherapeutics after blood-brain barrier disruption: where are we now, and where we are going. J Neurooncol 2020;(147):261-278.
78. Hadjipanayis CG, Widhalm G, Stummer W. What is the surgical benefit of utilizing 5-aminolevulinic acid for fluorescence-guided surgery of malignant gliomas? Neurosurgery 2015;(77):663-673.
79. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 2000;(93):1003-1013.
80. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomized controlled multicentre phase III trial. Lancet Oncol 2006;(7):392-401.
81. Gandhi S, Tayebi Meybodi A, Belykh E, et al. Survival outcomes among patients with high-grade glioma treated with 5-aminolevulinic acide guided surgery: a systematic review and meta-analysis. Front Oncol 2019;(9):620.
82. Schucht P, Knittel S, Slotboom J, et al. 5-ALA complete resections go beyond MR contrast enhancement: shift corrected volumetric analysis of the extent of resection in surgery for glioblastoma. Acta Neurochir (Wien) 2014;(156):305-312.
83. Stummer W, Tonn J-C, Goetz C, et al. 5-Aminolevulinic acid-derived tumor fluorescence: the diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and postoperative imaging. Neurosurgery 2014;(74):310-320.
84. Richter JCO, Haj-Hosseini N, Hallbeck M, Wårdell K. Combination of hand-held probe and microscopy for fluorescence guided surgery in the brain tumor marginal zone. Photodiagnosis Photodyn Ther 2017;(18):185-192.
85. Widhalm G, Kiesel B, Woehrer A, et al. 5-aminolevulinic acid induced fluorescence is a powerful intraoperative marker for precise histopathological grading of gliomas with non-significant contrast-enhancement. PLoS One 2013;(8): e76988.
86. Jaber M, Wölfer J, Ewelt C, et al. The value of 5-aminolevulinic acid in low-grade gliomas and high-grade gliomas lacking glioblastoma imaging features: an analysis based on fluorescence, magnetic resonance imaging, 18f-fluoroethyltyrosine positron emission tomography, and tumor molecular factors. Neurosurgery 2016;(78):401-411.
87. Smith EJ, Gohil K, Thompson CM, Naik A, Hassaneen W. Fluorescein-Guided Resection of High-Grade Gliomas: A Meta-Analysis. World Neurosurg 2021;(4): S1878-8750(21)01314-0.
88. La Rocca G, Sabatino G, Menna G, Altieri R, Ius T, Marchese E, Olivi A, Barresi V, Della Pepa G.M. 5-Aminolevulinic Acid False Positives in Cerebral Neuro-Oncology: Not All That Is Fluorescent Is Tumor. A Case-Based Update and Literature Review. World Neurosurg 2020;(137):187-193.
89. Nestler U, Warter A, Cabre P, Manzo N. A case of late-onset multiple sclerosis mimicking glioblastoma and displaying intraoperative 5-aminolevulinic acid fluorescence. Acta Neurochir (Wien) 2012;(154):899-901.
90. Miyatake S, Kuroiwa T, Kajimoto Y, Miyashita M, Tanaka H, Tsuji M. Fluorescence of non-neoplastic, magnetic resonance imaging enhancing tissue by 5-aminolevulinic acid: case report. Neurosurgery 2007;(61):E1101-E1103 [discussion: E1103-110].
91. Voellger B, Klein J, Mawrin C, Firsching R. 5-Aminolevulinic acid (5-ALA) fluorescence in infectious disease of the brain. Acta Neurochir (Wien) 2014; (156):1977-1978.
92. Solis WG, Hansen M. Fluorescence in a cryptococcoma following administration of 5-aminolevulinic acid hydrochloride (Gliolan). BMJ Case Rep 2017;(11);2017: bcr2017219469.
93. Omoto K, Matsuda R, Nakagawa I, Motoyama Y, Nakase H. False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: a case-report. Surg Neurol Int 2018;(9):49.
94. de Laurentis C, Del Bene M, Fociani P, Tonello C, Pollo B, DiMeco F. 5-ALA fluorescence in case of brain abscess by Aggregatibacter mimicking glioblastoma. World Neurosurg 2019;(125):175-1.
95. Picart T, Berhouma M, Dumot C, Pallud J, Metellus P, Armoiry X, Guyotat J. Optimization of high-grade glioma resection using 5-ALA fluorescence-guided surgery: A literature review and practical recommendations from the neuro-oncology club of the French society of neurosurgery. Neurochirurgie 2019;65(4):164-177.
96. Valle R.D, Hadjipanayis C.G, Stummer W. Established and emerging uses of 5-ALA in the brain: an overview. Neurooncol 2019;141(3):487-494.
97. Stepp H, Stummer W. 5-ALA in the management of malignant glioma. Lasers Surg Med 2018;50(5):399-419.
98. Hollon T, Stummer W, Orringer D, Molina E.S. Surgical Adjuncts to Increase the Extent of Resection: Intraoperative MRI, Fluorescence, and Raman Histology. Neurosurg Clin N Am 2019;30(1):65-74.
99. Kamp M.A, Molle Z.K, Munoz-Bendix C, Rapp M, Sabel M, Steiger H-J, Cornelius J.F. Various shades of red-a systematic analysis of qualitative estimation of ALA-derived fluorescence in neurosurgery. Neurosurg Rev 2018;41(1):3-18.
100. Leuthardt EC, Lim CCH, Shah MN, et al. Use of movable high-field-strength intraoperative magnetic resonance imaging with awake craniotomies for resection of gliomas: preliminary experience. Neurosurgery 2011;(69):194-205.
101. Li P, Qian R, Niu C, Fu X. Impact of intraoperative MRI-guided resection on resection and survival in patient with gliomas: a meta-analysis. Current medical research and opinion 2017;33(4):621-630.
102. Marongiu A, D'Andrea G, Raco A. 1.5-T Field Intraoperative Magnetic Resonance Imaging Improves Extent of Resection and Survival in Glioblastoma Removal. World neurosurgery 2017;(98):578-586.
103. Coburger J, Segovia von Riehm J, Ganslandt O, Wirtz CR, Renovanz M. Is There an Indication for Intraoperative MRI in Subtotal Resection of Glioblastoma? A Multicenter Retrospective Comparative Analysis. World neurosurgery 2018;(110): e389-e397.
104. Familiari P, Frati A, Pesce A, Miscusi M, Cimatti M, Raco A. Real Impact of Intraoperative Magnetic Resonance Imaging in Newly Diagnosed Glioblastoma Multiforme Resection: An Observational Analytic Cohort Study from a Single Surgeon Experience. World neurosurgery 2018;(116): e9-e17.
105. Makary M, Chiocca EA, Erminy N, Antor M, Bergese SD, Abdel-Rasoul M, et al. Clinical and economic outcomes of low-field intraoperative MRI-guided tumor resection neurosurgery. Journal of magnetic resonance imaging: JMRI 2011;34(5):1022-1030.
106. Ranganathan P, Pramesh CS, Aggarwal R. Common pitfalls in statistical analysis: Absolute risk reduction, relative risk reduction, and number needed to treat. Perspectives in clinical research 2016;7(1):51-53.
107. Gousias K, Markou M, Voulgaris S, Goussia A, Voulgari P, Bai M, et al. Descriptive epidemiology of cerebral gliomas in northwest Greece and study of potential predisposing factors, 2005-2007. Neuroepidemiology 2009;33(2):89-95.
108. Uyl-de Groot CA, Stupp R, van der Bent M. Cost-effectiveness of temozolomide for the treatment of newly diagnosed glioblastoma multiforme. Expert review of pharmaco-economics & outcomes research 2009;9(3):235-241.
109. Martikainen JA, Kivioja A, Hallinen T, Vihinen P. Economic evaluation of temozolomide in the treatment of recurrent glioblastoma multiforme. Pharmaco Economics 2005;23(8):803-815.
110. Garside R, Pitt M, Anderson R, Rogers G, Dyer M, Mealing S, et al. The effectiveness and cost-effectiveness of carmustine implants and temozolomide for the treatment of newly diagnosed high-grade glioma: a systematic review and economic evaluation. Health technology assessment 2007;11(45): iii-iv, ix-221.
111. Messali A, Hay JW, Villacorta R. The cost-effectiveness of temozolomide in the adjuvant treatment of newly diagnosed glioblastoma in the United States. Neuro-oncology 2013;15(11):1532-1542.
112. Brauer CA, Rosen AB, Olchanski NV, Neumann PJ. Cost-utility analyses in orthopaedic surgery. The Journal of bone and joint surgery American volume 2005;87(6):1253-1259.
113. Sachs JD, Ahluwalia IJ, K.Y. A, E. A, D. C, Z. D, et al. Macroeconomics and Health: Investing in Health for Economic Development. November 2001.
114. Li Y, Ali S, Clarke J, Cha S. Bevacizumab in Recurrent Glioma: Patterns of Treatment Failure and Implications. Brain tumor research and treatment 2017;5(1):1-9.
115. Kovic B, Xie F. Economic Evaluation of Bevacizumab for the First-Line Treatment of Newly Diagnosed Glioblastoma Multiforme. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2015;33(20):2296-2302.
116. Eljamel MS, Mahboob SO. The effectiveness and cost-effectiveness of intraoperative imaging in high-grade glioma resection; a comparative review of intraoperative ALA, fluorescein, ultrasound and MRI. Photodiagnosis and photodynamic therapy 2016;(16):35-43.
117. Enchev Y. Neuronavigation: geneology, reality, and prospects. Neurosurg Focus. 2009;(27): E11.