Characterizing white matter fiber orientation effects on multi-parametric quantitative BOLD assessment of oxygen extraction fraction

Kaczmarz, Stephan; Göttler, Jens; Zimmer, Claus; Hyder, Fahmeed; Preibisch, Christine

doi:10.1177/0271678x19839502

Cited by 23 publications

(33 citation statements)

References 63 publications

(246 reference statements)

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“…The model assumes that the system is in the static dephasing regime [ 58 ] whereby OEF is predominantly weighted to the medium sized and larger venules and provides an average blood oxygenation within the entire vasculature. Additionally, hemosiderin or protein accumulations, background gradients, white matter fiber orientation, and contrast agent leakage could bias the OEF estimation [ 59 , 60 , 61 ]. Finally, the number of patients was relatively small which was related to our rather strict inclusion/exclusion criteria (e.g., IDH mutation status, standard treatment only).…”

Section: Discussionmentioning

confidence: 99%

Hypoxia and Microvascular Alterations Are Early Predictors of IDH-Mutated Anaplastic Glioma Recurrence

Stadlbauer

Oberndorfer

Heinz

et al. 2021

Cancers

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Anaplastic gliomas (AG) represents aggressive brain tumors that often affect young adults. Although isocitrate-dehydrogenase (IDH) gene mutation has been identified as a more favorable prognostic factor, most IDH-mutated AG patients are confronted with tumor recurrence. Hence, increased knowledge about pathophysiological precursors of AG recurrence is urgently needed in order to develop precise diagnostic monitoring and tailored therapeutic approaches. In this study, 142 physiological magnetic resonance imaging (phyMRI) follow-up examinations in 60 AG patients after standard therapy were evaluated and magnetic resonance imaging (MRI) biomarker maps for microvascular architecture and perfusion, neovascularization activity, oxygen metabolism, and hypoxia calculated. From these 60 patients, 34 patients developed recurrence of the AG, and 26 patients showed no signs for AG recurrence during the study period. The time courses of MRI biomarker changes were analyzed regarding early pathophysiological alterations over a one-year period before radiological AG recurrence or a one-year period of stable disease for patients without recurrence, respectively. We detected intensifying local tissue hypoxia 250 days prior to radiological recurrence which initiated upregulation of neovascularization activity 50 to 70 days later. These changes were associated with a switch from an avascular infiltrative to a vascularized proliferative phenotype of the tumor cells another 30 days later. The dynamic changes of blood perfusion, microvessel density, neovascularization activity, and oxygen metabolism showed a close physiological interplay in the one-year period prior to radiological recurrence of IDH-mutated AG. These findings may path the wave for implementing both new MR-based imaging modalities for routine follow-up monitoring of AG patients after standard therapy and furthermore may support the development of novel, tailored therapy options in recurrent AG.

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Section: Discussionmentioning

confidence: 99%

Hypoxia and Microvascular Alterations Are Early Predictors of IDH-Mutated Anaplastic Glioma Recurrence

Stadlbauer

Oberndorfer

Heinz

et al. 2021

Cancers

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“… 48 Although vessel orientation effects in WM have been observed, 88 recently, reasonably low orientation-related errors of mq-BOLD were demonstrated in WM. 89 …”

Section: Discussionmentioning

confidence: 99%

“…48 Although vessel orientation effects in WM have been observed, 88 recently, reasonably low orientation-related errors of mq-BOLD were demonstrated in WM. 89 Future multi-center studies -such as the CREST-H study 75 -are clearly necessary to further resolve current limitations and to gain an even deeper understanding of the hemodynamic impairments in ICAS. Finally, improvement in the treatment guidelines could be achieved by considering perfusion and oxygen sensitive biomarkers.…”

Section: Applicability and Limitationsmentioning

confidence: 99%

Hemodynamic impairments within individual watershed areas in asymptomatic carotid artery stenosis by multimodal MRI

Kaczmarz

Göttler

Petr

et al. 2020

J Cereb Blood Flow Metab

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Improved understanding of complex hemodynamic impairments in asymptomatic internal carotid artery stenosis (ICAS) is crucial to better assess stroke risks. Multimodal MRI is ideal for measuring brain hemodynamics and has the potential to improve diagnostics and treatment selections. We applied MRI-based perfusion and oxygenation-sensitive imaging in ICAS with the hypothesis that the sensitivity to hemodynamic impairments will improve within individual watershed areas (iWSA). We studied cerebral blood flow (CBF), cerebrovascular reactivity (CVR), relative cerebral blood volume (rCBV), relative oxygen extraction fraction (rOEF), oxygen extraction capacity (OEC) and capillary transit-time heterogeneity (CTH) in 29 patients with asymptomatic, unilateral ICAS (age 70.3 ± 7.0 y) and 30 age-matched healthy controls. In ICAS, we found significant impairments of CBF, CVR, rCBV, OEC, and CTH (strongest lateralization ΔCVR = –24%), but not of rOEF. Although the spatial overlap of compromised hemodynamic parameters within each patient varied in a complex manner, most pronounced changes of CBF, CVR and rCBV were detected within iWSAs (strongest effect ΔCVR = +117%). At the same time, CTH impairments were iWSA independent, indicating widespread dysfunction of capillary-level oxygen diffusivity. In summary, complementary MRI-based perfusion and oxygenation parameters offer deeper perspectives on complex microvascular impairments in individual patients. Furthermore, knowledge about iWSAs improves the sensitivity to hemodynamic impairments.

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“…As the qBOLD model assumes that the ASE signal is localised to deoxyhaemoglobin, the additional signal contribution of myelin is not accounted for in the qBOLD model and will lead to error in the final oxygenation parameter estimates. This has previously been shown to have an influence on the estimates of OEF and DBV made using mp-qBOLD (Kaczmarz et al, 2019).…”

Section: White Mattermentioning

confidence: 96%

“…In reality, dephasing may also be driven by several non-blood sources of magnetic susceptibility present in the brain. This is particularly relevant in white matter (WM) where the reliability of qBOLD measurements have recently been called into question (Kaczmarz et al, 2019). Axons, within WM fibre bundles, are wrapped in myelin, which is known to possess strong diamagnetic susceptibility (Wharton and Bowtell, 2012).…”

Section: Additional Sources Of Magnetic Susceptibilitymentioning

confidence: 99%

Improving qBOLD based measures of oxygen extraction fraction using hyperoxia-BOLD derived measures of blood volume

Stone

Blockley

2020

Preprint

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1Streamlined-qBOLD (sqBOLD) is a recently proposed refinement of the quantitative 2 BOLD (qBOLD) technique capable of producing non-invasive and quantitative maps 3 of oxygen extraction fraction (OEF) in a clinically feasible scan time. However, 4 sqBOLD measurements of OEF have been reported as being systematically lower 5 than expected in healthy brain. Since the qBOLD framework infers OEF from the 6 ratio of the reversible transverse relaxation rate (R2′) and deoxygenated blood 7 volume (DBV), this underestimation of OEF has been largely attributed to an 8 overestimation of DBV made using this technique. 9 10This study proposes a novel method, hyperoxia-constrained qBOLD (hqBOLD), to 11 improve sqBOLD estimates of OEF. This method circumvents difficulties associated 12 with inferring DBV from the qBOLD model by replacing it with a separate 13 measurement of blood volume derived from hyperoxia-BOLD contrast. In a group of 14 ten healthy volunteers, hqBOLD produced measurements of OEF in cortical grey 15 matter (OEFhqBOLD = 44.7 ± 11.9 %) that were in better agreement with global 16 oximetry measures (OEFTRUST = 40.4 ± 7.7 %), compared to sqBOLD derived 17 measures (OEFsqBOLD = 13.1 ± 4.0 %). 19However, in the same group hqBOLD measures of OEF were found to be outside 20 the physiological range in white matter regions (> 100%). By deriving maps of 21 simulated R2′ from TRUST and hyperoxia-BOLD imaging data, the hqBOLD 22 overestimation of OEF in white matter was hypothesised to originate from additional sources of magnetic susceptibility beyond deoxyhaemoglobin that are present in 1 white matter. Introduction:1 Oxygen extraction fraction (OEF) is an important indicator of the metabolic function 2 of brain tissue that describes the fraction of oxygen removed from arterial blood to 3 serve oxidative metabolism. Imaging methods capable of providing non-invasive 4 parametric maps of OEF can provide key regional information that allows the 5 metabolic profile of brain tissue to be characterised, having applications in the 6 investigation of brain function and disease. Streamlined-quantitative BOLD 7 (sqBOLD) (Stone and Blockley, 2017) is a recently proposed refinement of the 8 quantitative BOLD (qBOLD) (An and Lin, 2003; He and Yablonskiy, 2007; Yablonskiy 9 et al., 2013) technique capable of noninvasively and quantitatively mapping OEF on 10 a regional level. This technique has been shown to be clinically relevant (Stone et 11 al., 2019a), producing parametric maps of tissue oxygenation in clinically appropriate 12 scan times.13 14 DBV overestimation 15 However, the measurements of OEF made using sqBOLD have been observed to be 16 lower than expected compared to generally accepted literature values (OEFsqBOLD ~ 17 20%, OEFliterature ~ 30 -40%) (Stone and Blockley, 2017). This underestimation in 18 OEF has largely been attributed to a systematic overestimation in the sqBOLD 19 measurement of deoxygenated blood volume (DBV). There are several potential 20 confounds in the sqBOLD measurement of DBV, including signal fr...

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Characterizing white matter fiber orientation effects on multi-parametric quantitative BOLD assessment of oxygen extraction fraction

Cited by 23 publications

References 63 publications

Hypoxia and Microvascular Alterations Are Early Predictors of IDH-Mutated Anaplastic Glioma Recurrence

Hypoxia and Microvascular Alterations Are Early Predictors of IDH-Mutated Anaplastic Glioma Recurrence

Hemodynamic impairments within individual watershed areas in asymptomatic carotid artery stenosis by multimodal MRI

Improving qBOLD based measures of oxygen extraction fraction using hyperoxia-BOLD derived measures of blood volume

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