Feasibility of glioblastoma tissue response mapping with physiologic BOLD imaging using precise oxygen and carbon dioxide challenge.


Journal

Magma (New York, N.Y.)
ISSN: 1352-8661
Titre abrégé: MAGMA
Pays: Germany
ID NLM: 9310752

Informations de publication

Date de publication:
Feb 2022
Historique:
received: 29 06 2021
accepted: 19 11 2021
revised: 15 11 2021
pubmed: 8 12 2021
medline: 11 3 2022
entrez: 7 12 2021
Statut: ppublish

Résumé

Innovative physiologic MRI development focuses on depiction of heterogenous vascular and metabolic features in glioblastoma. For this feasibility study, we employed blood oxygenation level-dependent (BOLD) MRI with standardized and precise carbon dioxide (CO Seven newly diagnosed untreated patients with suspected glioblastoma were prospectively included to undergo a BOLD study with combined CO Quantification of BOLD signal change after gas challenges can be used to identify specific responses to standardized stimuli in glioblastoma patients. Integration of this approach with automatic VOI segmentation grants improved characterization of tumor subzones and edema. Magnitude of BOLD signal change during the 3 stimuli can be visualized at voxel precision through color-coded maps overlayed onto whole brain and identified VOIs. Our preliminary investigation shows good feasibility of BOLD with standardized and precise CO

Identifiants

pubmed: 34874499
doi: 10.1007/s10334-021-00980-7
pii: 10.1007/s10334-021-00980-7
doi:

Substances chimiques

Carbon Dioxide 142M471B3J
Oxygen S88TT14065

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

29-44

Subventions

Organisme : krebsforschung schweiz
ID : KFS-3975-08-2016-R

Informations de copyright

© 2021. The Author(s), under exclusive licence to European Society for Magnetic Resonance in Medicine and Biology (ESMRMB).

Références

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 (2020) EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol. https://doi.org/10.1038/s41571-020-00447-z
doi: 10.1038/s41571-020-00447-z pubmed: 33293629 pmcid: 7904519
Wen PY, Weller M, Lee EQ, Alexander BM, Barnholtz-Sloan JS, Barthel FP, Batchelor TT, Bindra RS, Chang SM, Chiocca EA, Cloughesy TF, DeGroot JF, Galanis E, Gilbert MR, Hegi ME, Horbinski C, Huang RY, Lassman AB, Le Rhun E, Lim M, Mehta MP, Mellinghoff IK, Minniti G, Nathanson D, Platten M, Preusser M, Roth P, Sanson M, Schiff D, Short SC, Taphoorn MJB, Tonn J-C, Tsang J, Verhaak RGW, von Deimling A, Wick W, Zadeh G, Reardon DA, Aldape KD, van den Bent MJ (2020) Glioblastoma in adults: a Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions. Neuro Oncol 22:1073–1113
pubmed: 32328653 pmcid: 7594557
Lim M, Xia Y, Bettegowda C, Weller M (2018) Current state of immunotherapy for glioblastoma. Nat Rev Clin Oncol 15:422–442
pubmed: 29643471
Le Rhun E, Preusser M, Roth P, Reardon DA, van den Bent M, Wen P, Reifenberger G, Weller M (2019) Molecular targeted therapy of glioblastoma. Cancer Treat Rev 80:101896
pubmed: 31541850
Ellingson BM (2014) Radiogenomics and imaging phenotypes in glioblastoma: novel observations and correlation with molecular characteristics. Curr Neurol Neurosci Rep 15:506
Mazurowski MA (2015) Radiogenomics: what it is and why it is important. J Am Coll Radiol 12:862–866
pubmed: 26250979
Singh G, Manjila S, Sakla N, True A, Wardeh AH, Beig N, Vaysberg A, Matthews J, Prasanna P, Spektor V (2021) Radiomics and radiogenomics in gliomas: a contemporary update. Br J Cancer. https://doi.org/10.1038/s41416-021-01387-w
doi: 10.1038/s41416-021-01387-w pubmed: 34876674 pmcid: 8405677
Clement P, Booth T, Borovečki F, Emblem KE, Figueiredo P, Hirschler L, Jančálek R, Keil VC, Maumet C, Özsunar Y, Pernet C, Petr J, Pinto J, Smits M, Warnert EAH (2021) GliMR: cross-border collaborations to promote advanced MRI biomarkers for glioma. J Med Biol Eng 41:115–125
Hu LS, Hawkins-Daarud A, Wang L, Li J, Swanson KR (2020) Imaging of intratumoral heterogeneity in high-grade glioma. Cancer Lett 477:97–106
pubmed: 32112907 pmcid: 7108976
Shiroishi MS, Boxerman JL, Pope WB (2015) Physiologic MRI for assessment of response to therapy and prognosis in glioblastoma. Neuro Oncol 18:467–478
pubmed: 26364321 pmcid: 4799679
Hyare H, Thust S, Rees J (2017) Advanced MRI techniques in the monitoring of treatment of gliomas. Curr Treat Options Neurol 19:11
pubmed: 28349351
Boxerman JL, Quarles CC, Hu LS, Erickson BJ, Gerstner ER, Smits M, Kaufmann TJ, Barboriak DP, Huang RH, Wick W, Weller M, Galanis E, Kalpathy-Cramer J, Shankar L, Jacobs P, Chung C, van den Bent MJ, Chang S, Al Yung WK, Cloughesy TF, Wen PY, Gilbert MR, Rosen BR, Ellingson BM, Schmainda KM, Committee JBTDDCISS, Arons DF, Kingston A, Sandak D, Wallace M, Musella A, Haynes C (2020) Consensus recommendations for a dynamic susceptibility contrast MRI protocol for use in high-grade gliomas. Neuro Oncol 22:1262–1275
pubmed: 32516388 pmcid: 7523451
Boxerman JL, Shiroishi MS, Ellingson BM, Pope WB (2016) Dynamic susceptibility contrast MR imaging in glioma: review of current clinical practice. Magn Reson Imaging Clin N Am 24:649–670
pubmed: 27742108
Zhang J, Liu H, Tong H, Wang S, Yang Y, Liu G, Zhang W (2017) Clinical applications of contrast-enhanced perfusion MRI techniques in gliomas: recent advances and current challenges. Contrast Media Mol Imaging 2017:e7064120
Arevalo-Perez J, Peck KK, Young RJ, Holodny AI, Karimi S, Lyo JK (2015) Dynamic contrast-enhanced perfusion MRI and diffusion-weighted imaging in grading of gliomas. J Neuroimaging 25:792–798
pubmed: 25867683
Alsaedi A, Doniselli F, Jäger HR, Panovska-Griffiths J, Rojas-Garcia A, Golay X, Bisdas S (2019) The value of arterial spin labelling in adults glioma grading: systematic review and meta-analysis. Oncotarget 10:1589–1601
pubmed: 30899427 pmcid: 6422184
Falk Delgado A, De Luca F, van Westen D, Falk Delgado A (2018) Arterial spin labeling MR imaging for differentiation between high- and low-grade glioma—a meta-analysis. Neuro Oncol 20:1450–1461
pubmed: 29868920 pmcid: 6176798
Togao O, Hiwatashi A, Yamashita K, Kikuchi K, Mizoguchi M, Yoshimoto K, Suzuki SO, Iwaki T, Obara M, Van Cauteren M, Honda H (2016) Differentiation of high-grade and low-grade diffuse gliomas by intravoxel incoherent motion MR imaging. Neuro Oncol 18:132–141
pubmed: 26243792
Castellano A, Bailo M, Cicone F, Carideo L, Quartuccio N, Mortini P, Falini A, Cascini GL, Minniti G (2021) Advanced imaging techniques for radiotherapy planning of gliomas. Cancers 13:1063
pubmed: 33802292 pmcid: 7959155
Ellingson BM, Bendszus M, Boxerman J, Barboriak D, Erickson BJ, Smits M, Nelson SJ, Gerstner E, Alexander B, Goldmacher G, Wick W, Vogelbaum M, Weller M, Galanis E, Kalpathy-Cramer J, Shankar L, Jacobs P, Pope WB, Yang D, Chung C, Knopp MV, Cha S, van den Bent MJ, Chang S, Al Yung WK, Cloughesy TF, Wen PY, Gilbert MR, the Jumpstarting Brain Tumor Drug Development Coalition Imaging Standardization Steering Committee, Whitney A, Sandak D, Musella A, Haynes C, Wallace M, Arons DF, Kingston A, Sul J, Krainak D, the Jumpstarting Brain Tumor Drug Development Coalition Imaging Standardization Steering Committee (2015) Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials. Neuro Oncol 17:1188–1198
pubmed: 26250565 pmcid: 4588759
Verburg N, Koopman T, Yaqub MM, Hoekstra OS, Lammertsma AA, Barkhof F, Pouwels PJW, Reijneveld JC, Heimans JJ, Rozemuller AJM, Bruynzeel AME, Lagerwaard F, Vandertop WP, Boellaard R, Wesseling P, de Witt Hamer PC (2020) Improved detection of diffuse glioma infiltration with imaging combinations: a diagnostic accuracy study. Neuro Oncol 22:412–422
pubmed: 31550353
Suh CH, Kim HS, Jung SC, Choi CG, Kim SJ (2018) 2-Hydroxyglutarate MR spectroscopy for prediction of isocitrate dehydrogenase mutant glioma: a systemic review and meta-analysis using individual patient data. Neuro Oncol 20:1573–1583
pubmed: 30020513 pmcid: 6231199
Paech D, Windschuh J, Oberhollenzer J, Dreher C, Sahm F, Meissner J-E, Goerke S, Schuenke P, Zaiss M, Regnery S, Bickelhaupt S, Bäumer P, Bendszus M, Wick W, Unterberg A, Bachert P, Ladd ME, Schlemmer H-P, Radbruch A (2018) Assessing the predictability of IDH mutation and MGMT methylation status in glioma patients using relaxation-compensated multipool CEST MRI at 7.0 T. Neuro Oncol 20:1661–1671
pubmed: 29733378 pmcid: 6231210
Englander ZK, Horenstein CI, Bowden SG, Chow DS, Otten ML, Lignelli A, Bruce JN, Canoll P, Grinband J (2018) Extent of BOLD vascular dysregulation is greater in diffuse gliomas without isocitrate dehydrogenase 1 R132H mutation. Radiology 287:965–972
pubmed: 29369751
Stadlbauer A, Zimmermann M, Heinz G, Oberndorfer S, Doerfler A, Buchfelder M, Rössler K (2017) Magnetic resonance imaging biomarkers for clinical routine assessment of microvascular architecture in glioma. J Cereb Blood Flow Metab 37:632–643
pubmed: 27317652
Stadlbauer A, Zimmermann M, Doerfler A, Oberndorfer S, Buchfelder M, Coras R, Kitzwögerer M, Roessler K (2018) Intratumoral heterogeneity of oxygen metabolism and neovascularization uncovers 2 survival-relevant subgroups of IDH1 wild-type glioblastoma. Neuro Oncol 20:1536–1546
pubmed: 29718366 pmcid: 6176796
Goerke S, Soehngen Y, Deshmane A, Zaiss M, Breitling J, Boyd PS, Herz K, Zimmermann F, Klika KD, Schlemmer H-P, Paech D, Ladd ME, Bachert P (2019) Relaxation-compensated APT and rNOE CEST-MRI of human brain tumors at 3 T. Magn Reson Med 82:622–632
pubmed: 30927313
Leao DJ, Craig PG, Godoy LF, Leite CC, Policeni B (2020) Response assessment in neuro-oncology criteria for gliomas: practical approach using conventional and advanced techniques. Am J Neuroradiol 41:10–20
pubmed: 31857322 pmcid: 6975322
Ellingson BM, Wen PY, Cloughesy TF (2018) Evidence and context of use for contrast enhancement as a surrogate of disease burden and treatment response in malignant glioma. Neuro Oncol 20:457–471
pubmed: 29040703
Sebök M, van Niftrik CHB, Muscas G, Pangalu A, Seystahl K, Weller M, Regli L, Fierstra J (2021) Hypermetabolism and impaired cerebrovascular reactivity beyond the standard MRI-identified tumor border indicate diffuse glioma extended tissue infiltration. Neuro Oncol Adv. https://doi.org/10.1093/noajnl/vdab048
doi: 10.1093/noajnl/vdab048
Shaikh F, Dupont-Roettger D, Dehmeshki J, Awan O, Kubassova O, Bisdas S (2020) The role of imaging biomarkers derived from advanced imaging and radiomics in the management of brain tumors. Front Oncol. https://doi.org/10.3389/fonc.2020.559946
doi: 10.3389/fonc.2020.559946 pubmed: 33738243 pmcid: 7539039
Strauss SB, Meng A, Ebani EJ, Chiang GC (2019) Imaging glioblastoma posttreatment: progression, pseudoprogression, pseudoresponse, radiation necrosis. Radiol Clin North Am 57:1199–1216
pubmed: 31582045
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:e6828396
Muscas G, van Niftrik CHB, Sebök M, Della Puppa A, Seystahl K, Andratschke N, Brown M, Weller M, Regli L, Piccirelli M, Fierstra J (2021) Distinct cerebrovascular reactivity patterns for brain radiation necrosis. Cancers 13:1840
pubmed: 33924308 pmcid: 8069508
Slessarev M, Han J, Mardimae A, Prisman E, Preiss D, Volgyesi G, Ansel C, Duffin J, Fisher JA (2007) Prospective targeting and control of end-tidal CO2 and O2 concentrations. J Physiol 581:1207–1219
pubmed: 17446225 pmcid: 2170842
Fierstra J, van Niftrik C, Piccirelli M, Bozinov O, Pangalu A, Krayenbühl N, Valavanis A, Weller M, Regli L (2018) Diffuse gliomas exhibit whole brain impaired cerebrovascular reactivity. Magn Reson Imaging 45:78–83
pubmed: 28986176
Muscas G, van Niftrik CHB, Sebök M, Seystahl K, Piccirelli M, Stippich C, Weller M, Regli L, Fierstra J (2020) Hemodynamic investigation of peritumoral impaired blood oxygenation-level dependent cerebrovascular reactivity in patients with diffuse glioma. Magn Reson Imaging 70:50–56
pubmed: 32302735
Fierstra J, van Niftrik B, Piccirelli M, Burkhardt JK, Pangalu A, Kocian R, Valavanis A, Weller M, Regli L, Bozinov O (2016) Altered intraoperative cerebrovascular reactivity in brain areas of high-grade glioma recurrence. Magn Reson Imaging 34:803–808
pubmed: 26968146
Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232–243
pubmed: 21068832 pmcid: 3206737
Watkins S, Robel S, Kimbrough IF, Robert SM, Ellis-Davies G, Sontheimer H (2014) Disruption of astrocyte–vascular coupling and the blood–brain barrier by invading glioma cells. Nat Commun 5:4196
pubmed: 24943270
Montgomery MK, Kim SH, Dovas A, Zhao HT, Goldberg AR, Xu W, Yagielski AJ, Cambareri MK, Patel KB, Mela A, Humala N, Thibodeaux DN, Shaik MA, Ma Y, Grinband J, Chow DS, Schevon C, Canoll P, Hillman EMC (2020) Glioma-induced alterations in neuronal activity and neurovascular coupling during disease progression. Cell Rep 31:107500
pubmed: 32294436 pmcid: 7443283
Bowden SG, Gill BJA, Englander ZK, Horenstein CI, Zanazzi G, Chang PD, Samanamud J, Lignelli A, Bruce JN, Canoll P, Grinband J (2018) Local glioma cells are associated with vascular dysregulation. AJNR Am J Neuroradiol 39:507–514
pubmed: 29371254 pmcid: 6060022
Iranmahboob A, Peck KK, Brennan NP, Karimi S, Fisicaro R, Hou B, Holodny AI (2016) Vascular reactivity maps in patients with gliomas using breath-holding BOLD fMRI. J Neuroimaging 26:232–239
pubmed: 26250554 pmcid: 5087143
Hsu Y-Y, Chang C-N, Jung S-M, Lim K-E, Huang J-C, Fang S-Y, Liu H-L (2004) Blood oxygenation level-dependent MRI of cerebral gliomas during breath holding. J Magn Reson Imaging 19:160–167
pubmed: 14745748
Holodny AI, Schulder M, Liu WC, Maldjian JA, Kalnin AJ (1999) Decreased BOLD functional MR activation of the motor and sensory cortices adjacent to a glioblastoma multiforme: implications for image-guided neurosurgery. Am J Neuroradiol 20:609–612
pubmed: 10319970 pmcid: 7056038
Holodny AI, Schulder M, Liu W-C, Wolko J, Maldjian JA, Kalnin AJ (2000) The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. Am J Neuroradiol 21:1415–1422
pubmed: 11003273 pmcid: 7974044
Corroyer-Dulmont A, Chakhoyan A, Collet S, Durand L, MacKenzie ET, Petit E, Bernaudin M, Touzani O, Valable S (2015) Imaging modalities to assess oxygen status in glioblastoma. Front Med. https://doi.org/10.3389/fmed.2015.00057
doi: 10.3389/fmed.2015.00057
Gérard M, Corroyer-Dulmont A, Lesueur P, Collet S, Chérel M, Bourgeois M, Stefan D, Limkin EJ, Perrio C, Guillamo J-S, Dubray B, Bernaudin M, Thariat J, Valable S (2019) Hypoxia imaging and adaptive radiotherapy: a state-of-the-art approach in the management of glioma. Front Med. https://doi.org/10.3389/fmed.2019.00117
doi: 10.3389/fmed.2019.00117
Virani N, Kwon J, Zhou H, Mason R, Berbeco R, Protti A (2021) In vivo hypoxia characterization using blood oxygen level dependent magnetic resonance imaging in a preclinical glioblastoma mouse model. Magn Reson Imaging 76:52–60
pubmed: 33220448
Christen T, Schmiedeskamp H, Straka M, Bammer R, Zaharchuk G (2012) Measuring brain oxygenation in humans using a multiparametric quantitative blood oxygenation level dependent MRI approach. Magn Reson Med 68:905–911
pubmed: 22162074
Christen T, Lemasson B, Pannetier N, Farion R, Remy C, Zaharchuk G, Barbier EL (2012) Is T2* enough to assess oxygenation? Quantitative blood oxygen level-dependent analysis in brain tumor. Radiology 262:495–502
pubmed: 22156990 pmcid: 3267079
Chédeville AL, Madureira PA (2021) The role of hypoxia in glioblastoma radiotherapy resistance. Cancers 13:542
pubmed: 33535436 pmcid: 7867045
Colwell N, Larion M, Giles AJ, Seldomridge AN, Sizdahkhani S, Gilbert MR, Park DM (2017) Hypoxia in the glioblastoma microenvironment: shaping the phenotype of cancer stem-like cells. Neuro Oncol 19:887–896
pubmed: 28339582 pmcid: 5570138
Mendichovszky I, Jackson A (2011) Imaging hypoxia in gliomas. BJR 84:S145–S158
pubmed: 22433825 pmcid: 3473902
Bekaert L, Valable S, Lechapt-Zalcman E, Ponte K, Collet S, Constans J-M, Levallet G, Bordji K, Petit E, Branger P, Emery E, Manrique A, Barré L, Bernaudin M, Guillamo J-S (2017) [18F]-FMISO PET study of hypoxia in gliomas before surgery: correlation with molecular markers of hypoxia and angiogenesis. Eur J Nucl Med Mol Imaging 44:1383–1392
pubmed: 28315948
Preibisch C, Shi K, Kluge A, Lukas M, Wiestler B, Göttler J, Gempt J, Ringel F, Jaberi MA, Schlegel J, Meyer B, Zimmer C, Pyka T, Förster S (2017) Characterizing hypoxia in human glioma: a simultaneous multimodal MRI and PET study. NMR Biomed 30:e3775
Stadlbauer A, Kinfe TM, Eyüpoglu I, Zimmermann M, Kitzwögerer M, Podar K, Buchfelder M, Heinz G, Oberndorfer S, Marhold F (2020) Tissue hypoxia and alterations in microvascular architecture predict glioblastoma recurrence in humans. Clin Cancer Res. https://doi.org/10.1158/1078-0432.CCR-20-3580
doi: 10.1158/1078-0432.CCR-20-3580 pubmed: 33293375
Stadlbauer A, Kinfe TM, Zimmermann M, Eyüpoglu I, Brandner N, Buchfelder M, Zaiss M, Dörfler A, Brandner S (2020) Association between tissue hypoxia, perfusion restrictions, and microvascular architecture alterations with lesion-induced impairment of neurovascular coupling. J Cereb Blood Flow Metab. https://doi.org/10.1177/0271678X20947546
doi: 10.1177/0271678X20947546 pubmed: 32787542
Vu C, Chai Y, Coloigner J, Nederveen AJ, Borzage M, Bush A, Wood JC (2021) Quantitative perfusion mapping with induced transient hypoxia using BOLD MRI. Magn Reson Med 85:168–181
pubmed: 32767413
MacDonald ME, Berman AJL, Mazerolle EL, Williams RJ, Pike GB (2018) Modeling hyperoxia-induced BOLD signal dynamics to estimate cerebral blood flow, volume and mean transit time. Neuroimage 178:461–474
pubmed: 29852282
Stieb S, Riesterer O, Boss A, Weiss T, Guckenberger M, Özbay PS, Nanz D, Rossi C (2019) Dependency of the blood oxygen level dependent-response to hyperoxic challenges on the order of gas administration in intracranial malignancies. Neuroradiology 61:783–793
pubmed: 30949747
Özbay PS, Stieb S, Rossi C, Riesterer O, Boss A, Weiss T, Kuhn FP, Pruessmann KP, Nanz D (2018) Lesion magnetic susceptibility response to hyperoxic challenge: a biomarker for malignant brain tumor microenvironment? Magn Reson Imaging 47:147–153
pubmed: 29221966
Bashat DB, Artzi M, Ami HB, Aizenstein O, Blumenthal DT, Bokstein F, Corn BW, Ram Z, Kanner AA, Lifschitz-Mercer B, Solar I, Kolatt T, Palmon M, Edrei Y, Abramovitch R (2012) Hemodynamic response imaging: a potential tool for the assessment of angiogenesis in brain tumors. PLoS ONE 7:e49416
pubmed: 23209575 pmcid: 3507885
Laufer S, Mazuz A, Nachmansson N, Fellig Y, Corn BW, Bokstein F, Bashat DB, Abramovitch R (2014) Monitoring brain tumor vascular heamodynamic following anti-angiogenic therapy with advanced magnetic resonance imaging in mice. PLoS ONE 9:e115093
pubmed: 25506833 pmcid: 4266643
Sobczyk O, Fierstra J, Venkatraghavan L, Poublanc J, Duffin J, Fisher JA, Mikulis DJ (2021) Measuring cerebrovascular reactivity: sixteen avoidable pitfalls. Front Physiol 12:990
Duffin J, Sobczyk O, Crawley AP, Poublanc J, Mikulis DJ, Fisher JA (2015) The dynamics of cerebrovascular reactivity shown with transfer function analysis. Neuroimage 114:207–216
pubmed: 25891374
van Niftrik CHB, Piccirelli M, Bozinov O, Pangalu A, Fisher JA, Valavanis A, Luft AR, Weller M, Regli L, Fierstra J (2017) Iterative analysis of cerebrovascular reactivity dynamic response by temporal decomposition. Brain Behav 7:e00705
pubmed: 28948064 pmcid: 5607533
Kassner A, Winter JD, Poublanc J, Mikulis DJ, Crawley AP (2010) Blood-oxygen level dependent MRI measures of cerebrovascular reactivity using a controlled respiratory challenge: reproducibility and gender differences. J Magn Reson Imaging 31:298–304
pubmed: 20099341
Fisher JA, Lashmi V, Mikulis DJ (2018) Magnetic resonance imaging-based cerebrovascular reactivity and hemodynamic reserve. Stroke 49:2011–2018
pubmed: 29986929
Delgado-López PD, Riñones-Mena E, Corrales-García EM (2018) Treatment-related changes in glioblastoma: a review on the controversies in response assessment criteria and the concepts of true progression, pseudoprogression, pseudoresponse and radionecrosis. Clin Transl Oncol 20:939–953
pubmed: 29218626
Lasocki A, Gaillard F (2019) Non-contrast-enhancing tumor: a new frontier in glioblastoma research. Am J Neuroradiol 40:758–765
pubmed: 30948373 pmcid: 7053910
Karschnia P, Vogelbaum MA, van den Bent M, Cahill DP, Bello L, Narita Y, Berger MS, Weller M, Tonn J-C (2021) Evidence-based recommendations on categories for extent of resection in diffuse glioma. Eur J Cancer 149:23–33
pubmed: 33819718
Niyazi M, Brada M, Chalmers AJ, Combs SE, Erridge SC, Fiorentino A, Grosu AL, Lagerwaard FJ, Minniti G, Mirimanoff R-O, Ricardi U, Short SC, Weber DC, Belka C (2016) ESTRO-ACROP guideline “target delineation of glioblastomas.” Radiother Oncol 118:35–42
pubmed: 26777122
Horská A, Barker PB (2010) Imaging of brain tumors: MR spectroscopy and metabolic imaging. Neuroimaging Clin N Am 20:293–310
pubmed: 20708548 pmcid: 2927327
Hakyemez B, Erdogan C, Bolca N, Yildirim N, Gokalp G, Parlak M (2006) Evaluation of different cerebral mass lesions by perfusion-weighted MR imaging. J Magn Reson Imaging 24:817–824
pubmed: 16958061
Di N, Cheng W, Chen H, Zhai F, Liu Y, Mu X, Chu Z, Lu N, Liu X, Wang B (2019) Utility of arterial spin labelling MRI for discriminating atypical high-grade glioma from primary central nervous system lymphoma. Clin Radiol 74:165.e1-165.e9
Xi Y, Kang X, Wang N, Liu T, Zhu Y, Cheng G, Wang K, Li C, Guo F, Yin H (2019) Differentiation of primary central nervous system lymphoma from high-grade glioma and brain metastasis using arterial spin labeling and dynamic contrast-enhanced magnetic resonance imaging. Eur J Radiol 112:59–64
pubmed: 30777220
Soni N, Srindharan K, Kumar S, Mishra P, Bathla G, Kalita J, Behari S (2018) Arterial spin labeling perfusion: prospective MR imaging in differentiating neoplastic from non-neoplastic intra-axial brain lesions. Neuroradiol J 31:544–553
pubmed: 29890916 pmcid: 6243465
Shah AH, Snelling B, Bregy A, Patel PR, Tememe D, Bhatia R, Sklar E, Komotar RJ (2013) Discriminating radiation necrosis from tumor progression in gliomas: a systematic review what is the best imaging modality? J Neurooncol 112:141–152
pubmed: 23344789
Wu H, Tong H, Du X, Guo H, Ma Q, Zhang Y, Zhou X, Liu H, Wang S, Fang J, Zhang W (2020) Vascular habitat analysis based on dynamic susceptibility contrast perfusion MRI predicts IDH mutation status and prognosis in high-grade gliomas. Eur Radiol 30:3254–3265
pubmed: 32078014
Pang H, Dang X, Ren Y, Zhuang D, Qiu T, Chen H, Zhang J, Ma N, Li G, Zhang J, Wu J, Feng X (2019) 3D-ASL perfusion correlates with VEGF expression and overall survival in glioma patients: comparison of quantitative perfusion and pathology on accurate spatial location-matched basis. J Magn Reson Imaging 50:209–220
pubmed: 30652410
Law M, Young RJ, Babb JS, Peccerelli N, Chheang S, Gruber ML, Miller DC, Golfinos JG, Zagzag D, Johnson G (2008) Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 247:490–498
pubmed: 18349315
Seeger A, Braun C, Skardelly M, Paulsen F, Schittenhelm J, Ernemann U, Bisdas S (2013) Comparison of three different MR perfusion techniques and MR spectroscopy for multiparametric assessment in distinguishing recurrent high-grade gliomas from stable disease. Acad Radiol 20:1557–1565
pubmed: 24200483
Dou W, Lin C-YE, Ding H, Shen Y, Dou C, Qian L, Wen B, Wu B (2019) Chemical exchange saturation transfer magnetic resonance imaging and its main and potential applications in pre-clinical and clinical studies. Quant Imaging Med Surg 9:1747766–1741766
Morrison MA, Lupo JM (2021) 7-T magnetic resonance imaging in the management of brain tumors. Magn Reson Imaging Clin N Am 29:83–102
pubmed: 33237018
Baudelet C (2005) Current issues in the utility of blood oxygen level dependent MRI for the assessment of modulations in tumor oxygenation. Curr Med Imaging 1:229–243
Losert C, Peller M, Schneider P, Reiser M (2002) Oxygen-enhanced MRI of the brain. Magn Reson Med 48:271–277
pubmed: 12210935
Fierstra J, Sobczyk O, Battisti-Charbonney A, Mandell DM, Poublanc J, Crawley AP, Mikulis DJ, Duffin J, Fisher JA (2013) Measuring cerebrovascular reactivity: what stimulus to use? J Physiol 591:5809–5821
pubmed: 24081155 pmcid: 3872753
Sebök M, van Niftrik CHB, Halter M, Hiller A, Seystahl K, Pangalu A, Weller M, Stippich C, Regli L, Fierstra J (2020) Crossed cerebellar diaschisis in patients with diffuse glioma is associated with impaired supratentorial cerebrovascular reactivity and worse clinical outcome. Cerebellum 19:824–832
pubmed: 32737798 pmcid: 7588366
Sobczyk O, Battisti-Charbonney A, Fierstra J, Mandell DM, Poublanc J, Crawley AP, Mikulis DJ, Duffin J, Fisher JA (2014) A conceptual model for CO2-induced redistribution of cerebral blood flow with experimental confirmation using BOLD MRI. Neuroimage 92:56–68
pubmed: 24508647
Lüdemann L, Förschler A, Grieger W, Zimmer C (2006) BOLD signal in the motor cortex shows a correlation with the blood volume of brain tumors. J Magn Reson Imaging 23:435–443
pubmed: 16506145
Johnston AJ, Steiner LA, Gupta AK, Menon DK (2003) Cerebral oxygen vasoreactivity and cerebral tissue oxygen reactivity† †AJJ is supported by an unrestricted neurosciences intensive care research grant from Codman. LAS is supported by grants from the Margarete und Walter Lichtenstein-Stiftung (Basel, Switzerland), a Myron B. Laver Grant (Department of Anaesthesia, University of Basel, Switzerland) and the Swiss National Science Foundation, and is recipient of an Overseas Research Student Award (Committee of Vice-Chancellors and Principals of the Universities of the United Kingdom). Br J Anaesth 90:774–786
pubmed: 12765894
Bickler PE, Feiner JR, Lipnick MS, Batchelder P, MacLeod DB, Severinghaus JW (2017) Effects of acute, profound hypoxia on healthy humans: implications for safety of tests evaluating pulse oximetry or tissue oximetry performance. Anesth Analg 124:146–153
pubmed: 27529318
Moreton FC, Dani KA, Goutcher C, O’Hare K, Muir KW (2016) Respiratory challenge MRI: practical aspects. NeuroImage Clin 11:667–677
pubmed: 27330967 pmcid: 4901170
Schwarzbauer C, Deichmann R (2012) Vascular component analysis of hyperoxic and hypercapnic BOLD contrast. Neuroimage 59:2401–2412
pubmed: 21945792
Song Y, Cho G, Chun S-I, Baek JH, Cho H, Kim YR, Park SB, Kim JK (2014) Oxygen-induced frequency shifts in hyperoxia: a significant component of BOLD signal. NMR Biomed 27:835–842
pubmed: 24828299
Ma Y, Berman AJL, Pike GB (2016) The effect of dissolved oxygen on the relaxation rates of blood plasma: Implications for hyperoxia calibrated BOLD. Magn Reson Med 76:1905–1911
pubmed: 26628286
Bonekamp D, Mouridsen K, Radbruch A, Kurz FT, Eidel O, Wick A, Schlemmer H-P, Wick W, Bendszus M, Østergaard L, Kickingereder P (2017) Assessment of tumor oxygenation and its impact on treatment response in bevacizumab-treated recurrent glioblastoma. J Cereb Blood Flow Metab 37:485–494
pubmed: 26861817
Fisher JA, Mikulis DJ (2021) Cerebrovascular reactivity: purpose, optimizing methods, and limitations to interpretation—a personal 20-year Odyssey of (Re)searching. Front Physiol. https://doi.org/10.3389/fphys.2021.629651
doi: 10.3389/fphys.2021.629651 pubmed: 35211030 pmcid: 8446542
Willie CK, Macleod DB, Shaw AD, Smith KJ, Tzeng YC, Eves ND, Ikeda K, Graham J, Lewis NC, Day TA, Ainslie PN (2012) Regional brain blood flow in man during acute changes in arterial blood gases. J Physiol 590:3261–3275
pubmed: 22495584 pmcid: 3459041
Willie CK, Tzeng Y-C, Fisher JA, Ainslie PN (2014) Integrative regulation of human brain blood flow. J Physiol 592:841–859
pubmed: 24396059 pmcid: 3948549
Hoiland RL, Bain AR, Rieger MG, Bailey DM, Ainslie PN (2015) Hypoxemia, oxygen content, and the regulation of cerebral blood flow. Am J Physiol Regul Integr Compar Physiol 310:R398–R413
Maralani PJ, Das S, Mainprize T, Phan N, Bharatha A, Keith J, Munoz DG, Sahgal A, Symons S, Ironside S, Faraji-Dana Z, Eilaghi A, Chan A, Alcaide-Leon P, Shearkhani O, Jakubovic R, Atenafu EG, Zaharchuk G, Mikulis D (2018) Hypoxia detection in infiltrative astrocytoma: ferumoxytol-based quantitative BOLD MRI with intraoperative and histologic validation. Radiology 288:821–829
pubmed: 29944077

Auteurs

Vittorio Stumpo (V)

Department of Neurosurgery, University Hospital Zurich, Frauenklinikstrasse 10, 8091, Zurich, Switzerland. vittorio.stumpo@usz.ch.
Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland. vittorio.stumpo@usz.ch.

Martina Sebök (M)

Department of Neurosurgery, University Hospital Zurich, Frauenklinikstrasse 10, 8091, Zurich, Switzerland.
Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Christiaan Hendrik Bas van Niftrik (CHB)

Department of Neurosurgery, University Hospital Zurich, Frauenklinikstrasse 10, 8091, Zurich, Switzerland.
Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Katharina Seystahl (K)

Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
Department of Neurology, University Hospital Zurich, Zurich, Switzerland.

Nicolin Hainc (N)

Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
Department of Neuroradiology, University Hospital Zurich, Zurich, Switzerland.

Zsolt Kulcsar (Z)

Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
Department of Neuroradiology, University Hospital Zurich, Zurich, Switzerland.

Michael Weller (M)

Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
Department of Neurology, University Hospital Zurich, Zurich, Switzerland.

Luca Regli (L)

Department of Neurosurgery, University Hospital Zurich, Frauenklinikstrasse 10, 8091, Zurich, Switzerland.
Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Jorn Fierstra (J)

Department of Neurosurgery, University Hospital Zurich, Frauenklinikstrasse 10, 8091, Zurich, Switzerland.
Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

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