Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging

Rijpkema, Mark; Kaanders, Johannes H.A.M.; Joosten, F.B.M.; Kogel, Albert J. van der; Heerschap, Arend

doi:10.1016/s0360-3016(02)02825-0

Cited by 106 publications

(91 citation statements)

References 54 publications

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“…The number of echoes used herein was a result of using in‐phase fat and water signal with echoes acquired with the same gradient polarity, together with SNR threshold. Previous clinical

T_{2}^{*}

studies have employed between 4 and 16 echo times 19, 39, 40. In this study, the signal acquired with the gradient echo sequence was found to be dominated by noise for echo times longer than 30 msec.…”

Section: Discussionmentioning

confidence: 73%

“…Median

T_{2}^{*}

values were calculated for each VOI and used to assess the quantitative repeatability, to account for a skewed parameter distribution previously described in the literature 15, 19. First, the Shapiro‐Wilk test was used to ascertain normality of the sample

T_{2}^{*}

distribution.…”

Section: Methodsmentioning

confidence: 99%

“…An increase in

T_{2}^{*}

was found to correlate with inhalation of higher percentages of oxygen in preclinical studies, but the magnitude of signal changes was not proportional to the absolute measured tissue oxygenation 16. Preclinical and clinical studies in prostate, cervix, and head and neck cancers have consistently reported increases in tumor tissue

T_{2}^{*}

in response to hyperoxic gas challenge 17, 18, 19, 20…”

mentioning

confidence: 99%

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Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Panek

Welsh

Dunlop

et al. 2016

Magnetic Resonance Imaging

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PurposeTo determine whether quantitation of T2* is sufficiently repeatable and sensitive to detect clinically relevant oxygenation levels in head and neck squamous cell carcinoma (HNSCC) at 3T.Materials and MethodsTen patients with newly diagnosed locally advanced HNSCC underwent two magnetic resonance imaging (MRI) scans between 24 and 168 hours apart prior to chemoradiotherapy treatment. A multiple gradient echo sequence was used to calculate T2* maps. A quadratic function was used to model the blood transverse relaxation rate as a function of blood oxygenation. A set of published coefficients measured at 3T were incorporated to account for tissue hematocrit levels and used to plot the dependence of fractional blood oxygenation (Y) on T2* values, together with the corresponding repeatability range. Repeatability of T2* using Bland–Altman analysis, and calculation of limits of agreement (LoA), was used to assess the sensitivity, defined as the minimum difference in fractional blood oxygenation that can be confidently detected.Results T2* LoA for 22 outlined tumor volumes were 13%. The T2* dependence of fractional blood oxygenation increases monotonically, resulting in increasing sensitivity of the method with increasing blood oxygenation. For fractional blood oxygenation values above 0.11, changes in T2* were sufficient to detect differences in blood oxygenation greater than 10% (Δ T2* > LoA for ΔY > 0.1).ConclusionQuantitation of T2* at 3T can detect clinically relevant changes in tumor oxygenation within a wide range of blood volumes and oxygen tensions, including levels reported in HNSCC. J. Magn. Reson. Imaging 2016;44:72–80.

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“…The number of echoes used herein was a result of using in‐phase fat and water signal with echoes acquired with the same gradient polarity, together with SNR threshold. Previous clinical

T_{2}^{*}

Section: Discussionmentioning

confidence: 73%

“…Median

T_{2}^{*}

T_{2}^{*}

distribution.…”

Section: Methodsmentioning

confidence: 99%

“…An increase in

T_{2}^{*}

T_{2}^{*}

in response to hyperoxic gas challenge 17, 18, 19, 20…”

mentioning

confidence: 99%

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Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Panek

Welsh

Dunlop

et al. 2016

Magnetic Resonance Imaging

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“…The high clinical impact of this method in oncologic applications is underlined by numerous animal studies investigating tumor hypoxia (2,3,(16)(17)(18) and vessel maturation and function (19)(20)(21). The feasibility of respiratory challenges in clinical settings has been further demonstrated in several tumor studies in humans (22)(23)(24)(25)(26)(27).The response to hyperoxia and hypercapnia, affecting both oxygenation and blood flow and volume, can be measured using magnetic resonance imaging (MRI), because the related changes in deoxyhemoglobin concentration (dHb) ultimately manifest in changes in the reversible transverse relaxation rate R* 2 (1,28), a relation that is known as the blood-oxygenation-level-dependent (BOLD) effect (29). Furthermore, an increased blood flow also leads to an accelerated inflow of unsaturated spins in slice-selective MR sequences.…”

mentioning

confidence: 98%

Quantification of the magnetic resonance signal response to dynamic (C)O₂‐enhanced imaging in the brain at 3 T: R*₂ BOLD vs. balanced SSFP

Remmele

Dahnke

Flacke

et al. 2010

Magnetic Resonance Imaging

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Purpose: To compare two magnetic resonance (MR) contrast mechanisms, R* 2 BOLD and balanced SSFP, for the dynamic monitoring of the cerebral response to (C)O 2 respiratory challenges. Materials and Methods:Carbogen and CO 2 -enriched air were delivered to 9 healthy volunteers and 1 glioblastoma patient. The cerebral response was recorded by twodimensional (2D) dynamic multi-gradient-echo and passband-balanced steady-state free precession (bSSFP) sequences, and local changes of R* 2 and signal intensity were investigated. Detection sensitivity was analyzed by statistical tests. An exponential signal model was fitted to the global response function delivered by each sequence, enabling quantitative comparison of the amplitude and temporal behavior. Results:The bSSFP signal changes during carbogen and CO 2 /air inhalation were lower compared with R* 2 BOLD (ca. 5% as opposed to 8-13%). The blood-oxygen-level-dependent (BOLD) response amplitude enabled differentiation between carbogen and CO 2 /air by a factor of 1.4-1.6, in contrast to bSSFP, where differentiation was not possible. Furthermore, motion robustness and detection sensitivity were higher for R* 2 BOLD.Conclusion: Both contrast mechanisms are well suited to dynamic (C)O 2 -enhanced MR imaging, although the R* 2 BOLD mechanism was demonstrated to be superior in several respects for the chosen application. This study suggests that the R* 2 BOLD and bSSFP-response characteristics are related to different physiologic mechanisms. THE MEASUREMENT of the magnetic resonance (MR) response to respiratory challenges that induce elevated levels of O 2 (hyperoxia) and CO 2 (hypercapnia) has been shown to provide insight into a wide range of physiologic parameters: MR-monitored respiratory challenges have been applied to noninvasively assess blood and tissue oxygenation (1-5) and cerebrovascular reactivity to CO 2 -enriched (6-12) and O 2 -enriched (13-15) blood levels. The high clinical impact of this method in oncologic applications is underlined by numerous animal studies investigating tumor hypoxia (2,3,(16)(17)(18) and vessel maturation and function (19)(20)(21). The feasibility of respiratory challenges in clinical settings has been further demonstrated in several tumor studies in humans (22)(23)(24)(25)(26)(27).The response to hyperoxia and hypercapnia, affecting both oxygenation and blood flow and volume, can be measured using magnetic resonance imaging (MRI), because the related changes in deoxyhemoglobin concentration (dHb) ultimately manifest in changes in the reversible transverse relaxation rate R* 2 (1,28), a relation that is known as the blood-oxygenation-level-dependent (BOLD) effect (29). Furthermore, an increased blood flow also leads to an accelerated inflow of unsaturated spins in slice-selective MR sequences. This results in an apparent increase of the longitudinal relaxation rate, R 1 , when using high flip angles, short repetition times, or steady-state sequences (30).The classic approach to detecting the response to hyperoxia or hypercapnia with...

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“…Recent studies showed that carbogen in combination with nicotinamide can increase tumor oxygenation and therefore improve efficacy of radiotherapy (7). BOLD MRI has been successfully used in monitoring the efficacy of these tumor-oxygenating regimens in radiotherapy (8).…”

mentioning

confidence: 99%

Influence of body temperature on the BOLD effect in murine SCC tumors†

Reijnders

English

Krishna

et al. 2004

Magnetic Resonance in Med

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Changes in the blood oxygen level dependent (BOLD) enhancements in tumors (squamous cell carcinoma, (SCCVII)) implanted in mice maintained at core temperatures of 30°C or 37°C were measured using MRI and compared to tumor oxygen levels obtained using an oxygen-sensitive Eppendorf electrode. Tumors were implanted in a hindleg of the mice intramuscularly. Tumor-bearing mice were imaged by BOLD MRI, while first breathing air and then carbogen (95% O 2 , 5% CO 2 ) for 15-min intervals at a core temperature of 30°C. After an equilibration period, the identical regimen was conducted with the same animal maintained at 37°C. This procedure was repeated with additional mice starting at 37°C followed by imaging at 30°C. Likewise, oxygen electrode measurements of the tumor were determined at core temperatures of 30°C and 37°C. The Eppendorf measurements showed that tumors in animals maintained at 30°C were significantly more hypoxic than at 37°C. MRI studies demonstrated stronger BOLD enhancement at 30°C than at 37°C, suggesting significant changes in hypoxia and/or blood flow in tumors at these temperatures. The findings of the study stress the importance of maintaining normal core temperature when assessing tumor oxygen status using functional imaging modalities or oxygen-sensitive electrodes.

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Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging

Cited by 106 publications

References 54 publications

Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Quantification of the magnetic resonance signal response to dynamic (C)O₂‐enhanced imaging in the brain at 3 T: R*₂ BOLD vs. balanced SSFP

Influence of body temperature on the BOLD effect in murine SCC tumors†

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Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging

Cited by 106 publications

References 54 publications

Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Repeatability and sensitivity of measurements in patients with head and neck squamous cell carcinoma at 3T

Quantification of the magnetic resonance signal response to dynamic (C)O2‐enhanced imaging in the brain at 3 T: R*2 BOLD vs. balanced SSFP

Influence of body temperature on the BOLD effect in murine SCC tumors†

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Quantification of the magnetic resonance signal response to dynamic (C)O₂‐enhanced imaging in the brain at 3 T: R*₂ BOLD vs. balanced SSFP