The response of human tumors to carbogen breathing, monitored by gradient-recalled echo magnetic resonance imaging

Griffiths, John R.; Taylor, N. Jane; Howe, Franklyn A.; Saunders, Michele I.; Robinson, Simon P.; Hoskin, Peter; Powell, Melanie; Thoumine, Michelle; Caine, Linda A.; Baddeley, H.

doi:10.1016/s0360-3016(97)00326-x

Cited by 120 publications

(94 citation statements)

References 10 publications

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“…Although to our knowledge carbogen-induced changes in R 2 * from brain tumors have not been reported in patients, increases in SI consistent with a reduction in R 2 * in response to carbogen breathing have now been observed in a variety of human tumors (23,40). There has also been a report of BOLD imaging identifying in a patient a node that was undetected by conventional MRI (23).…”

Section: Magnitude Of the Bold Response To Carbogenmentioning

confidence: 79%

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Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Dunn

O’Hara

Wadghiri

et al. 2002

Magnetic Resonance Imaging

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Purpose: To examine, using blood oxygen level dependent (BOLD) MRI and EPR oximetry, the changes in oxygenation of intracranial tumors induced by carbogen breathing. Materials and Methods:The 9L and CNS-1 intracranial rat tumor models were imaged at 7T, before and during carbogen breathing, using a multi-echo gradient-echo (GE) sequence to map R 2 *. On a different group of 9L tumors, tissue pO 2 was measured using EPR oximetry with lithium phthalocyanine as the oxygen-sensitive material. Results:The average decline in R 2 * with carbogen breathing was 13 Ϯ 1 s -1 in the CNS-1 tumors and 29 Ϯ 4 s -1 in the 9L tumor. The SI vs. TE decay curves indicate the presence of multiple components in the tumor. Tissue pO 2 in the two 9L tumors measured was 8.6 Ϯ 0.5 and 3.6 Ϯ 0.6 mmHg during air breathing, and rose to 20 Ϯ 7 and 16 Ϯ 4 mmHg (mean Ϯ SE) with carbogen breathing. Significant changes were observed by 10 minutes, but changes in pO 2 and R 2 * continued in some subjects over the entire 40 minutes. Conclusion:EPR results indicate that glial sarcomas may be radiobiologically hypoxic. Both EPR and BOLD data indicate that carbogen breathing increases brain tumor oxygenation. These data support the use of BOLD imaging to monitor changes in oxygenation in brain tumors.

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Section: Magnitude Of the Bold Response To Carbogenmentioning

confidence: 79%

“…This imaging method has been used to indirectly assess oxygenation in both animal (14 -22) and human (23) tumors. BOLD MRI can have a high spatial resolution and is noninvasive, making it suitable for monitoring and characterizing tumors.…”

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confidence: 99%

Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Dunn

O’Hara

Wadghiri

et al. 2002

Magnetic Resonance Imaging

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“…102 Increases in tumor GRE (gradient recalled echo) image intensity have been reported during carbogen breathing and during hyperoxia. 63,65,[103][104][105][106][107][108][109][110] The main cause of the GRE image intensity change is the increase in blood oxygenation through the breathing of a high-oxygen-content gas, reducing the dHb concentration of tumor blood vessels. The increased blood oxygenation associated with carbogen breathing produces a decrease in R Ã 2 ð¼ 1=T Ã 2 Þ.…”

Section: Techniques For the Assessment Of Tumor Oxygenationmentioning

confidence: 99%

Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications

2004

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This review paper attempts to provide an overview of the principles and techniques that are often termed electron paramagnetic resonance (EPR) oximetry. The paper discusses the potential of such methods and illustrates they have been successfully applied to measure oxygen tension, an essential parameter of the tumor microenvironment. To help the reader understand the motivation for carrying out these measurements, the importance of tumor hypoxia is first discussed: the basic issues of why a tumor is hypoxic, why these hypoxic microenvironments promote processes driving malignant progression and why hypoxia dramatically influences the response of tumors to cytotoxic treatments will be explained. The different methods that have been used to estimate the oxygenation in tumors will be reviewed. To introduce the basics of EPR oximetry, the specificity of in vivo EPR will be discussed by comparing this technique with NMR and MRI. The different types of paramagnetic oxygen sensors will be presented, as well as the methods for recording the information (EPR spectroscopy, EPR imaging, dynamic nuclear polarization). Several applications of EPR for characterizing tumor oxygenation will be illustrated, with a special emphasis on pharmacological interventions that modulate the tumor microenvironment. Finally, the challenges for transposing the method into the clinic will also be discussed.

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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.…”

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confidence: 99%

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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The response of human tumors to carbogen breathing, monitored by gradient-recalled echo magnetic resonance imaging

Cited by 120 publications

References 10 publications

Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications

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

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The response of human tumors to carbogen breathing, monitored by gradient-recalled echo magnetic resonance imaging

Cited by 120 publications

References 10 publications

Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Changes in oxygenation of intracranial tumors with carbogen: A BOLD MRI and EPR oximetry study

Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications

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

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Product

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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