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Published in: Neurosurgical Review 2/2019

Open Access 01-06-2019 | Review

Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery—review of the literature

Authors: Eric Suero Molina, S. Schipmann, W. Stummer

Published in: Neurosurgical Review | Issue 2/2019

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Abstract

Malignant glioma surgery involves the challenge of preserving the neurological status of patients harboring these lesions while pursuing a maximal tumor resection, which is correlated with overall and progression-free survival. Presently, several tools exist for assisting neurosurgeons in visualizing malignant tissue. Fluorescence-guided surgery (FGS) with 5-aminolevulinic acid (5-ALA) has increasingly been used during the last decade for identifying malignant glioma. Intraoperative magnetic resonance imaging (iMRI), first introduced in the mid-1990s, is being evaluated as a further tool to maximize the extent of resection. We aimed to evaluate the literature and discuss synergies and differences between FGS with 5-ALA and iMRI. We conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement. After excluding non-relevant articles, 16 articles were evaluated and included in the qualitative analysis, comprising 2 (n = 2) reviews of the literatures, 1 (n = 1) book chapter, and 13 (n = 13) clinical articles. ALA-induced fluorescence goes beyond the borders of gadolinium contrast enhancement. Several studies stress the synergy between both tools, enabling increase in extent of resection. We point out advantages of combining both methods. iMRI, however, is not widely available, is expensive, and is not recommended as sole resection control tool in high-grade glioma. For these centers, FGS together with mapping and monitoring techniques, neuronavigation and, when needed, intraoperative ultrasound provides an excellent setting for achieving state-of-the-art gross total resection of high-grade gliomas.
Literature
1.
go back to reference Albert FK, Wirtz CR, Tronnier VM, Hamer J, Bonsanto MM, Staubert A, Knauth M, Kunze S (1998) Intraoperative diagnostic and interventional MRI in neurosurgery: first experience with an “open MR” system. In: Hellwig D, Bauer BL (eds) Minimally invasive techniques for neurosurgery: current status and future perspectives. Springer, Berlin, pp 229–235. https://doi.org/10.1007/978-3-642-58731-3_39 CrossRef Albert FK, Wirtz CR, Tronnier VM, Hamer J, Bonsanto MM, Staubert A, Knauth M, Kunze S (1998) Intraoperative diagnostic and interventional MRI in neurosurgery: first experience with an “open MR” system. In: Hellwig D, Bauer BL (eds) Minimally invasive techniques for neurosurgery: current status and future perspectives. Springer, Berlin, pp 229–235. https://​doi.​org/​10.​1007/​978-3-642-58731-3_​39 CrossRef
3.
5.
go back to reference Bergsneider M, Sehati N, Villablanca P, McArthur DL, Becker DP, Liau LM (2005) Mahaley clinical research award: extent of glioma resection using low-field (0.2 T) versus high-field (1.5 T) intraoperative MRI and image-guided frameless neuronavigation. Clin Neurosurg 52:389–399PubMed Bergsneider M, Sehati N, Villablanca P, McArthur DL, Becker DP, Liau LM (2005) Mahaley clinical research award: extent of glioma resection using low-field (0.2 T) versus high-field (1.5 T) intraoperative MRI and image-guided frameless neuronavigation. Clin Neurosurg 52:389–399PubMed
6.
go back to reference Black PM, Moriarty T, Alexander E 3rd, Stieg P, Woodard EJ, Gleason PL, Martin CH, Kikinis R, Schwartz RB, Jolesz FA (1997) Development and implementation of intraoperative magnetic resonance imaging and its neurosurgical applications. Neurosurgery 41:831–842 discussion 842-835CrossRefPubMed Black PM, Moriarty T, Alexander E 3rd, Stieg P, Woodard EJ, Gleason PL, Martin CH, Kikinis R, Schwartz RB, Jolesz FA (1997) Development and implementation of intraoperative magnetic resonance imaging and its neurosurgical applications. Neurosurgery 41:831–842 discussion 842-835CrossRefPubMed
9.
11.
go back to reference Coburger J, Merkel A, Scherer M, Schwartz F, Gessler F, Roder C, Pala A, Konig R, Bullinger L, Nagel G, Jungk C, Bisdas S, Nabavi A, Ganslandt O, Seifert V, Tatagiba M, Senft C, Mehdorn M, Unterberg AW, Rossler K, Wirtz CR (2016) Low-grade glioma surgery in intraoperative magnetic resonance imaging: results of a multicenter retrospective assessment of the German study group for intraoperative magnetic resonance imaging. Neurosurgery 78:775–786. https://doi.org/10.1227/NEU.0000000000001081 CrossRefPubMed Coburger J, Merkel A, Scherer M, Schwartz F, Gessler F, Roder C, Pala A, Konig R, Bullinger L, Nagel G, Jungk C, Bisdas S, Nabavi A, Ganslandt O, Seifert V, Tatagiba M, Senft C, Mehdorn M, Unterberg AW, Rossler K, Wirtz CR (2016) Low-grade glioma surgery in intraoperative magnetic resonance imaging: results of a multicenter retrospective assessment of the German study group for intraoperative magnetic resonance imaging. Neurosurgery 78:775–786. https://​doi.​org/​10.​1227/​NEU.​0000000000001081​ CrossRefPubMed
12.
go back to reference Coburger J, Scheuerle A, Pala A, Thal D, Wirtz CR, Konig R (2017) Histopathological insights on imaging results of intraoperative magnetic resonance imaging, 5-aminolevulinic acid, and intraoperative ultrasound in glioblastoma surgery. Neurosurgery. https://doi.org/10.1093/neuros/nyw143 Coburger J, Scheuerle A, Pala A, Thal D, Wirtz CR, Konig R (2017) Histopathological insights on imaging results of intraoperative magnetic resonance imaging, 5-aminolevulinic acid, and intraoperative ultrasound in glioblastoma surgery. Neurosurgery. https://​doi.​org/​10.​1093/​neuros/​nyw143
13.
go back to reference Coburger J, Wirtz CR, Konig RW (2017) Impact of extent of resection and recurrent surgery on clinical outcome and overall survival in a consecutive series of 170 patients for glioblastoma in intraoperative high field magnetic resonance imaging. J Neurosurg Sci 61:233–244. 10.23736/S0390-5616.16.03284-7 CrossRefPubMed Coburger J, Wirtz CR, Konig RW (2017) Impact of extent of resection and recurrent surgery on clinical outcome and overall survival in a consecutive series of 170 patients for glioblastoma in intraoperative high field magnetic resonance imaging. J Neurosurg Sci 61:233–244. 10.​23736/​S0390-5616.​16.​03284-7 CrossRefPubMed
15.
go back to reference Della Puppa A, De Pellegrin S, d'Avella E, Gioffre G, Rossetto M, Gerardi A, Lombardi G, Manara R, Munari M, Saladini M, Scienza R (2013) 5-Aminolevulinic acid (5-ALA) fluorescence guided surgery of high-grade gliomas in eloquent areas assisted by functional mapping. Our experience and review of the literature. Acta Neurochir (Wien) 155:965–972; discussion 972. https://doi.org/10.1007/s00701-013-1660-x CrossRef Della Puppa A, De Pellegrin S, d'Avella E, Gioffre G, Rossetto M, Gerardi A, Lombardi G, Manara R, Munari M, Saladini M, Scienza R (2013) 5-Aminolevulinic acid (5-ALA) fluorescence guided surgery of high-grade gliomas in eloquent areas assisted by functional mapping. Our experience and review of the literature. Acta Neurochir (Wien) 155:965–972; discussion 972. https://​doi.​org/​10.​1007/​s00701-013-1660-x CrossRef
17.
go back to reference Diez Valle R, Tejada Solis S, Idoate Gastearena MA, Garcia de Eulate R, Dominguez Echavarri P, Aristu Mendiroz J (2011) Surgery guided by 5-aminolevulinic fluorescence in glioblastoma: volumetric analysis of extent of resection in single-center experience. J Neuro-Oncol 102:105–113. https://doi.org/10.1007/s11060-010-0296-4 CrossRef Diez Valle R, Tejada Solis S, Idoate Gastearena MA, Garcia de Eulate R, Dominguez Echavarri P, Aristu Mendiroz J (2011) Surgery guided by 5-aminolevulinic fluorescence in glioblastoma: volumetric analysis of extent of resection in single-center experience. J Neuro-Oncol 102:105–113. https://​doi.​org/​10.​1007/​s11060-010-0296-4 CrossRef
24.
go back to reference Feigl GC, Ritz R, Moraes M, Klein J, Ramina K, Gharabaghi A, Krischek B, Danz S, Bornemann A, Liebsch M, Tatagiba MS (2010) Resection of malignant brain tumors in eloquent cortical areas: a new multimodal approach combining 5-aminolevulinic acid and intraoperative monitoring. J Neurosurg 113:352–357. https://doi.org/10.3171/2009.10.JNS09447 CrossRefPubMed Feigl GC, Ritz R, Moraes M, Klein J, Ramina K, Gharabaghi A, Krischek B, Danz S, Bornemann A, Liebsch M, Tatagiba MS (2010) Resection of malignant brain tumors in eloquent cortical areas: a new multimodal approach combining 5-aminolevulinic acid and intraoperative monitoring. J Neurosurg 113:352–357. https://​doi.​org/​10.​3171/​2009.​10.​JNS09447 CrossRefPubMed
26.
31.
go back to reference Hefti M, von Campe G, Moschopulos M, Siegner A, Looser H, Landolt H (2008) 5-Aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institutuion. Swiss Med Wkly 138:180–185PubMed Hefti M, von Campe G, Moschopulos M, Siegner A, Looser H, Landolt H (2008) 5-Aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institutuion. Swiss Med Wkly 138:180–185PubMed
32.
go back to reference Hess KR (1999) Extent of resection as a prognostic variable in the treatment of gliomas. J Neuro-Oncol 42:227–231CrossRef Hess KR (1999) Extent of resection as a prognostic variable in the treatment of gliomas. J Neuro-Oncol 42:227–231CrossRef
35.
go back to reference Jaber M, Wolfer J, Ewelt C, Holling M, Hasselblatt M, Niederstadt T, Zoubi T, Weckesser M, Stummer W (2016) 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-fluoroethyl tyrosine positron emission tomography, and tumor molecular factors. Neurosurgery 78:401–411; discussion 411. https://doi.org/10.1227/NEU.0000000000001020 CrossRefPubMed Jaber M, Wolfer J, Ewelt C, Holling M, Hasselblatt M, Niederstadt T, Zoubi T, Weckesser M, Stummer W (2016) 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-fluoroethyl tyrosine positron emission tomography, and tumor molecular factors. Neurosurgery 78:401–411; discussion 411. https://​doi.​org/​10.​1227/​NEU.​0000000000001020​ CrossRefPubMed
50.
go back to reference Nickel K, Renovanz M, Konig J, Stockelmaier L, Hickmann AK, Nadji-Ohl M, Engelke J, Weimann E, Freudenstein D, Ganslandt O, Bullinger L, Wirtz CR, Coburger J (2017) 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. https://doi.org/10.1007/s10143-017-0836-x Nickel K, Renovanz M, Konig J, Stockelmaier L, Hickmann AK, Nadji-Ohl M, Engelke J, Weimann E, Freudenstein D, Ganslandt O, Bullinger L, Wirtz CR, Coburger J (2017) 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. https://​doi.​org/​10.​1007/​s10143-017-0836-x
59.
go back to reference Saito T, Muragaki Y, Maruyama T, Tamura M, Nitta M, Okada Y (2015) Intraoperative functional mapping and monitoring during glioma surgery. Neurol Med Chir (Tokyo) 55(Suppl 1):1–13CrossRef Saito T, Muragaki Y, Maruyama T, Tamura M, Nitta M, Okada Y (2015) Intraoperative functional mapping and monitoring during glioma surgery. Neurol Med Chir (Tokyo) 55(Suppl 1):1–13CrossRef
60.
go back to reference Sala F, Lanteri P (2003) Brain surgery in motor areas: the invaluable assistance of intraoperative neurophysiological monitoring. J Neurosurg Sci 47:79–88PubMed Sala F, Lanteri P (2003) Brain surgery in motor areas: the invaluable assistance of intraoperative neurophysiological monitoring. J Neurosurg Sci 47:79–88PubMed
61.
66.
go back to reference Schucht P, Beck J, Abu-Isa J, Andereggen L, Murek M, Seidel K, Stieglitz L, Raabe A (2012) Gross total resection rates in contemporary glioblastoma surgery: results of an institutional protocol combining 5-aminolevulinic acid intraoperative fluorescence imaging and brain mapping. Neurosurgery 71:927–935; discussion 935-926. https://doi.org/10.1227/NEU.0b013e31826d1e6b CrossRefPubMed Schucht P, Beck J, Abu-Isa J, Andereggen L, Murek M, Seidel K, Stieglitz L, Raabe A (2012) Gross total resection rates in contemporary glioblastoma surgery: results of an institutional protocol combining 5-aminolevulinic acid intraoperative fluorescence imaging and brain mapping. Neurosurgery 71:927–935; discussion 935-926. https://​doi.​org/​10.​1227/​NEU.​0b013e31826d1e6b​ CrossRefPubMed
67.
76.
go back to reference Stummer W, Stepp H, Moller G, Ehrhardt A, Leonhard M, Reulen HJ (1998) Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir 140:995–1000CrossRefPubMed Stummer W, Stepp H, Moller G, Ehrhardt A, Leonhard M, Reulen HJ (1998) Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir 140:995–1000CrossRefPubMed
77.
go back to reference Stummer W, Stocker S, Novotny A, Heimann A, Sauer O, Kempski O, Plesnila N, Wietzorrek J, Reulen HJ (1998) In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to 5-aminolevulinic acid. J Photochem Photobiol B 45:160–169CrossRefPubMed Stummer W, Stocker S, Novotny A, Heimann A, Sauer O, Kempski O, Plesnila N, Wietzorrek J, Reulen HJ (1998) In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to 5-aminolevulinic acid. J Photochem Photobiol B 45:160–169CrossRefPubMed
78.
go back to reference Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ (1998) Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 42:518–525 discussion 525-516CrossRefPubMed Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ (1998) Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 42:518–525 discussion 525-516CrossRefPubMed
79.
go back to reference Stummer W, Tonn JC, Goetz C, Ullrich W, Stepp H, Bink A, Pietsch T, Pichlmeier U (2014) 5-Aminolevulinic acid-derived tumor fluorescence: the diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and postoperative imaging. Neurosurgery 74:310–319; discussion 319-320. https://doi.org/10.1227/NEU.0000000000000267 CrossRefPubMed Stummer W, Tonn JC, Goetz C, Ullrich W, Stepp H, Bink A, Pietsch T, Pichlmeier U (2014) 5-Aminolevulinic acid-derived tumor fluorescence: the diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and postoperative imaging. Neurosurgery 74:310–319; discussion 319-320. https://​doi.​org/​10.​1227/​NEU.​0000000000000267​ CrossRefPubMed
80.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. https://doi.org/10.1056/NEJMoa043330 CrossRefPubMed Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. https://​doi.​org/​10.​1056/​NEJMoa043330 CrossRefPubMed
81.
go back to reference Talacchi A, Turazzi S, Locatelli F, Sala F, Beltramello A, Alessandrini F, Manganotti P, Lanteri P, Gambin R, Ganau M, Tramontano V, Santini B, Gerosa M (2010) Surgical treatment of high-grade gliomas in motor areas. The impact of different supportive technologies: a 171-patient series. J Neuro-Oncol 100:417–426. https://doi.org/10.1007/s11060-010-0193-x CrossRef Talacchi A, Turazzi S, Locatelli F, Sala F, Beltramello A, Alessandrini F, Manganotti P, Lanteri P, Gambin R, Ganau M, Tramontano V, Santini B, Gerosa M (2010) Surgical treatment of high-grade gliomas in motor areas. The impact of different supportive technologies: a 171-patient series. J Neuro-Oncol 100:417–426. https://​doi.​org/​10.​1007/​s11060-010-0193-x CrossRef
86.
go back to reference Widhalm G, Wolfsberger S, Minchev G, Woehrer A, Krssak M, Czech T, Prayer D, Asenbaum S, Hainfellner JA, Knosp E (2010) 5-Aminolevulinic acid is a promising marker for detection of anaplastic foci in diffusely infiltrating gliomas with nonsignificant contrast enhancement. Cancer 116:1545–1552. https://doi.org/10.1002/cncr.24903 CrossRefPubMed Widhalm G, Wolfsberger S, Minchev G, Woehrer A, Krssak M, Czech T, Prayer D, Asenbaum S, Hainfellner JA, Knosp E (2010) 5-Aminolevulinic acid is a promising marker for detection of anaplastic foci in diffusely infiltrating gliomas with nonsignificant contrast enhancement. Cancer 116:1545–1552. https://​doi.​org/​10.​1002/​cncr.​24903 CrossRefPubMed
87.
go back to reference Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, Tronnier VM (2000) Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 46:1112–1120 discussion 1120-1112CrossRefPubMed Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, Tronnier VM (2000) Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 46:1112–1120 discussion 1120-1112CrossRefPubMed
Metadata
Title
Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery—review of the literature
Authors
Eric Suero Molina
S. Schipmann
W. Stummer
Publication date
01-06-2019
Publisher
Springer Berlin Heidelberg
Published in
Neurosurgical Review / Issue 2/2019
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI
https://doi.org/10.1007/s10143-017-0907-z

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