Dynamic functional imaging of brain glucose utilization using fPET-FDG

Villien, Marjorie; Wey, Hsiao-Ying; Mandeville, Joseph B.; Catana, Ciprian; Polimeni, Jonathan R.; Sander, Christin Y.; Zürcher, Nicole R.; Chonde, Daniel B.; Fowler, Joanna S.; Rosen, Bruce R.; Hooker, Jacob M.

doi:10.1016/j.neuroimage.2014.06.025

Title: Dynamic functional imaging of brain glucose utilization using fPET-FDG

Abstract

We report that glucose is the principal source of energy for the brain and yet the dynamic response of glucose utilization to changes in brain activity is still not fully understood. Positron emission tomography (PET) allows quantitative measurement of glucose metabolism using 2-[18F]-fluorodeoxyglucose (FDG). However, FDG PET in its current form provides an integral (or average) of glucose consumption over tens of minutes and lacks the temporal information to capture physiological alterations associated with changes in brain activity induced by tasks or drug challenges. Traditionally, changes in glucose utilization are inferred by comparing two separate scans, which significantly limits the utility of the method. We report a novel method to track changes in FDG metabolism dynamically, with higher temporal resolution than exists to date and within a single session. Using a constant infusion of FDG, we demonstrate that our technique (termed fPET-FDG) can be used in an analysis pipeline similar to fMRI to define within-session differential metabolic responses. We use visual stimulation to demonstrate the feasibility of this method. Ultimately, this new method has a great potential to be used in research protocols and clinical settings since fPET-FDG imaging can be performed with most PET scanners and data acquisition andmore »« less

Authors:

Villien, Marjorie ^[1]; Wey, Hsiao-Ying ^[1]; Mandeville, Joseph B. ^[1]; Catana, Ciprian ^[1]; Polimeni, Jonathan R. ^[1]; Sander, Christin Y. ^[2]; Zürcher, Nicole R. ^[1]; Chonde, Daniel B. ^[1]; Fowler, Joanna S. ^[3]; Rosen, Bruce R. ^[4]; Hooker, Jacob M. ^[5]

Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Electrical Engineering and Computer Science
Brookhaven National Lab. (BNL), Upton, NY (United States). Biosciences Dept.
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Harvard-Massachusetts Institute of Technology, Cambridge, MA (United States). Division of Health Sciences and Technology
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Brookhaven National Lab. (BNL), Upton, NY (United States). Biosciences Dept.

Publication Date:: Sat Jun 14 00:00:00 EDT 2014

Research Org.:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE; National Institutes of Health (NIH)

OSTI Identifier:: 1281964

Grant/Contract Number:: SC0008430; P41EB015896; S10RR019933; R01EB014894

Resource Type:: Accepted Manuscript

Journal Name:: NeuroImage

Additional Journal Information:: Journal Volume: 100; Journal Issue: C; Journal ID: ISSN 1053-8119

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; 47 OTHER INSTRUMENTATION; 2-[18F]-fluorodeoxyglucose (FDG); Glucose utilization; Visual stimulus; MR/PET; PET

Citation Formats


                    Villien, Marjorie, Wey, Hsiao-Ying, Mandeville, Joseph B., Catana, Ciprian, Polimeni, Jonathan R., Sander, Christin Y., Zürcher, Nicole R., Chonde, Daniel B., Fowler, Joanna S., Rosen, Bruce R., and Hooker, Jacob M. Dynamic functional imaging of brain glucose utilization using fPET-FDG.  United States: N. p., 2014. 
Web.  doi:10.1016/j.neuroimage.2014.06.025.

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                    Villien, Marjorie, Wey, Hsiao-Ying, Mandeville, Joseph B., Catana, Ciprian, Polimeni, Jonathan R., Sander, Christin Y., Zürcher, Nicole R., Chonde, Daniel B., Fowler, Joanna S., Rosen, Bruce R., & Hooker, Jacob M. Dynamic functional imaging of brain glucose utilization using fPET-FDG.  United States.  https://doi.org/10.1016/j.neuroimage.2014.06.025

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                    Villien, Marjorie, Wey, Hsiao-Ying, Mandeville, Joseph B., Catana, Ciprian, Polimeni, Jonathan R., Sander, Christin Y., Zürcher, Nicole R., Chonde, Daniel B., Fowler, Joanna S., Rosen, Bruce R., and Hooker, Jacob M. Sat .  
"Dynamic functional imaging of brain glucose utilization using fPET-FDG".  United States.  https://doi.org/10.1016/j.neuroimage.2014.06.025.  https://www.osti.gov/servlets/purl/1281964.

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@article{osti_1281964,

  title        = {Dynamic functional imaging of brain glucose utilization using fPET-FDG},

  author       = {Villien, Marjorie and Wey, Hsiao-Ying and Mandeville, Joseph B. and Catana, Ciprian and Polimeni, Jonathan R. and Sander, Christin Y. and Zürcher, Nicole R. and Chonde, Daniel B. and Fowler, Joanna S. and Rosen, Bruce R. and Hooker, Jacob M.},

  abstractNote = {We report that glucose is the principal source of energy for the brain and yet the dynamic response of glucose utilization to changes in brain activity is still not fully understood. Positron emission tomography (PET) allows quantitative measurement of glucose metabolism using 2-[18F]-fluorodeoxyglucose (FDG). However, FDG PET in its current form provides an integral (or average) of glucose consumption over tens of minutes and lacks the temporal information to capture physiological alterations associated with changes in brain activity induced by tasks or drug challenges. Traditionally, changes in glucose utilization are inferred by comparing two separate scans, which significantly limits the utility of the method. We report a novel method to track changes in FDG metabolism dynamically, with higher temporal resolution than exists to date and within a single session. Using a constant infusion of FDG, we demonstrate that our technique (termed fPET-FDG) can be used in an analysis pipeline similar to fMRI to define within-session differential metabolic responses. We use visual stimulation to demonstrate the feasibility of this method. Ultimately, this new method has a great potential to be used in research protocols and clinical settings since fPET-FDG imaging can be performed with most PET scanners and data acquisition and analysis are straightforward. fPET-FDG is a highly complementary technique to MRI and provides a rich new way to observe functional changes in brain metabolism.},

  doi          = {10.1016/j.neuroimage.2014.06.025},

  journal      = {NeuroImage},

  number       = C,

  volume       = 100,

  place        = {United States},

  year         = {Sat Jun 14 00:00:00 EDT 2014},

  month        = {Sat Jun 14 00:00:00 EDT 2014}

}

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Effects of hyperglycemia on FDG-PET in patients with brain tumors

Journal Article Ishizu, K ; Nishizawa, S ; Yonekura, Y - Journal of Nuclear Medicine

In order to evaluate the effects of hyperglycemia on fluorodeoxyglucose (FDG) uptake in normal brain and brain tumors, we performed glucose loading during FDG-PET studies in 8 patients with brain tumors (7 gliomas and 1 metastatic tumor). Two FDG-PET studies were performed in all cases within a week; in control state and with glucose loading by intravenous infusion of 10% glucose solution. Serial arterial blood sampling was performed in all cases to obtain fractional uptake of FDG normalized by plasma integral of radioactivity (FU). On the static FDG images acquired from 40 to 60 minutes after FDG injection, regions ofmore »« less

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Title: Dynamic functional imaging of brain glucose utilization using fPET-FDG

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Glucose Metabolic Rate Kinetic Model Parameter Determination in Humans: The Lumped Constants and Rate Constants for [ 18 F]Fluorodeoxyglucose and [ 11 C]Deoxyglucose journal, June 1985

Human brain glucose metabolism may evolve during activation: Findings from a modified FDG PET paradigm journal, December 2006

Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. journal, June 1992

A Strategy for Removing the Bias in the Graphical Analysis Method journal, March 2001

Calibrated fMRI journal, August 2012

Functional mapping of the human visual cortex by magnetic resonance imaging journal, November 1991

FreeSurfer journal, August 2012

Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. journal, July 1992

The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. journal, January 1979

Comparison of Bolus and Infusion Methods for Receptor Quantitation: Application to [ 18 F]Cyclofoxy and Positron Emission Tomography journal, January 1993

Association between cerebral metabolic and structural abnormalities and cognitive performance in schizophrenia journal, August 2009

Changes in Relative Glucose Metabolic Rate Following Cortisol Administration in Aging Veterans with Posttraumatic Stress Disorder: An FDG-PET Neuroimaging Study journal, April 2009

Mapping human visual cortex with positron emission tomography journal, October 1986

Predicting efficacy of photodynamic therapy by real-time FDG-PET in a mouse tumour model journal, January 2012

THE [ 14 C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT journal, May 1977

Cerebral blood flow and glucose metabolism in healthy volunteers measured using a high-resolution PET scanner journal, January 2012

Cerebral metabolism and patterned visual Stimulation: A positron emission tomographic study of the human visual cortex journal, January 1988

Quantitative functional MRI: Concepts, issues and future challenges journal, August 2012

Concurrent CBF and CMRGlc changes during human brain activation by combined fMRI–PET scanning journal, November 2005

Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1 journal, October 2010

Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: Validation of method journal, November 1979

A receptor-based model for dopamine-induced fMRI signal journal, July 2013

Baseline CBF , and BOLD, CBF , and CMRO 2 fMRI of Visual and Vibrotactile Stimulations in Baboons journal, September 2010

The 18 F-fluorodeoxyglucose Lumped Constant Determined in Human Brain from Extraction Fractions of 18 F-fluorodeoxyglucose and Glucose journal, August 2001

Nonoxidative glucose consumption during focal physiologic neural activity journal, July 1988

Cocaine-Induced Redoppuction of Glucose Utilization in Human Brain: A Study Using Positron Emission Tomography and [Fluorine 18]-Fluorodeoxyglucose journal, June 1990

Brain work and Brain Imaging journal, July 2006

Dynamic models of BOLD contrast journal, August 2012

Effects of Chronic Cocaine Self-Administration on Cognition and Cerebral Glucose Utilization in Rhesus Monkeys journal, November 2012

Neurovascular coupling to D2/D3 dopamine receptor occupancy using simultaneous PET/functional MRI journal, May 2013

Influence of Plasma Glucose Concentration on Lumped Constant of the Deoxyglucose Method: Effects of Hyperglycemia in the Rat journal, November 1990

Translational MR Neuroimaging of Stroke and Recovery journal, August 2016

MR-PET head motion correction based on co-registration of multi-contrast MR images posted_content, January 2018

DREAMM: A Biobehavioral Imaging Methodology for Dynamic In Vivo Whole-Brain Mapping of Cell Type-Specific Functional Networks journal, December 2014

Combined PET/MRI: from Status Quo to Status Go. Summary Report of the Fifth International Workshop on PET/MR Imaging; February 15–19, 2016; Tübingen, Germany journal, August 2016

Functional dynamics of dopamine synthesis during monetary reward and punishment processing posted_content, December 2020

From simultaneous to synergistic MR‐PET brain imaging: A review of hybrid MR‐PET imaging methodologies journal, August 2018

Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus journal, September 2019

Functional dynamics of dopamine synthesis during monetary reward and punishment processing journal, May 2021

Simultaneous EEG–PET–fMRI measurements in disorders of consciousness: an exploratory study on diagnosis and prognosis journal, August 2017

Constant Infusion Radiotracer Administration for High Temporal Resolution Positron Emission Tomography (PET) of the Human Brain: Application to [18F]-Fluorodexoyglucose PET (FDG-PET) posted_content, June 2019

Analysis of continuous infusion functional PET (fPET) in the human brain journal, June 2020

Effects of flow changes on radiotracer binding: Simultaneous measurement of neuroreceptor binding and cerebral blood flow modulation journal, August 2017

Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex posted_content, October 2018

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images? journal, September 2017

The renaissance of functional 18F-FDG PET brain activation imaging journal, September 2018

Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex journal, April 2019

Imaging mitochondrial complex I activation during a vibrotactile stimulation: A PET study using [ 18 F]BCPP-EF in the conscious monkey brain journal, January 2020

Inflammation in Post-Traumatic Stress Disorder (PTSD): A Review of Potential Correlates of PTSD with a Neurological Perspective journal, January 2020

Evaluation of Task-Related Brain Activity: Is There a Role for 18 F FDG-PET Imaging? journal, July 2019

MR-PET head motion correction based on co-registration of multicontrast MR images journal, January 2019

Analysis of continuous infusion functional PET (fPET) in the human brain posted_content, September 2019

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images? text, January 2017

Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI posted_content, January 2019

Metabolite concentration changes associated with positive and negative BOLD responses in the human visual cortex: A functional MRS study at 7 Tesla journal, February 2019

Simultaneous PET-MRI imaging of cerebral blood flow and glucose metabolism in the symptomatic unilateral internal carotid artery/middle cerebral artery steno-occlusive disease journal, November 2019

Dynamic coupling between fMRI local connectivity and interictal EEG in focal epilepsy: A wavelet analysis approach: Dynamic Coupling between fMRI Local Connectivity and Interictal EEG in Focal Epilepsy journal, July 2017

Structure of the Human 4-Hydroxyphenylpyruvic Acid Dioxygenase Gene (HPD) journal, October 1994

Task-relevant brain networks identified with simultaneous PET/MR imaging of metabolism and connectivity journal, November 2017

Combined PET/MRI: from Status Quo to Status Go. Summary Report of the Fifth International Workshop on PET/MR Imaging; February 15–19, 2016; Tübingen, Germany journal, August 2016

MR-PET head motion correction based on co-registration of multi-contrast MR images posted_content, January 2018

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images? text, January 2017

The Effects of Capillary Transit Time Heterogeneity (CTH) on the Cerebral Uptake of Glucose and Glucose Analogs: Application to FDG and Comparison to Oxygen Uptake journal, October 2016

Inflammation in Post-Traumatic Stress Disorder (PTSD): A Review of Potential Correlates of PTSD with a Neurological Perspective journal, January 2020

Glucose Metabolic Rate Kinetic Model Parameter Determination in Humans: The Lumped Constants and Rate Constants for [ ¹⁸ F]Fluorodeoxyglucose and [ ¹¹ C]Deoxyglucose
journal, June 1985

Human brain glucose metabolism may evolve during activation: Findings from a modified FDG PET paradigm
journal, December 2006

Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation.
journal, June 1992

A Strategy for Removing the Bias in the Graphical Analysis Method
journal, March 2001

Calibrated fMRI
journal, August 2012

Functional mapping of the human visual cortex by magnetic resonance imaging
journal, November 1991

FreeSurfer
journal, August 2012

Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging.
journal, July 1992

The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man.
journal, January 1979

Comparison of Bolus and Infusion Methods for Receptor Quantitation: Application to [ ¹⁸ F]Cyclofoxy and Positron Emission Tomography
journal, January 1993

Association between cerebral metabolic and structural abnormalities and cognitive performance in schizophrenia
journal, August 2009

Changes in Relative Glucose Metabolic Rate Following Cortisol Administration in Aging Veterans with Posttraumatic Stress Disorder: An FDG-PET Neuroimaging Study
journal, April 2009

Mapping human visual cortex with positron emission tomography
journal, October 1986

Predicting efficacy of photodynamic therapy by real-time FDG-PET in a mouse tumour model
journal, January 2012

THE [ ¹⁴ C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT
journal, May 1977

Cerebral blood flow and glucose metabolism in healthy volunteers measured using a high-resolution PET scanner
journal, January 2012

Cerebral metabolism and patterned visual Stimulation: A positron emission tomographic study of the human visual cortex
journal, January 1988

Quantitative functional MRI: Concepts, issues and future challenges
journal, August 2012

Concurrent CBF and CMRGlc changes during human brain activation by combined fMRI–PET scanning
journal, November 2005

Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1
journal, October 2010

Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: Validation of method
journal, November 1979

A receptor-based model for dopamine-induced fMRI signal
journal, July 2013

Baseline CBF , and BOLD, CBF , and CMRO ₂ fMRI of Visual and Vibrotactile Stimulations in Baboons
journal, September 2010

The ¹⁸ F-fluorodeoxyglucose Lumped Constant Determined in Human Brain from Extraction Fractions of ¹⁸ F-fluorodeoxyglucose and Glucose
journal, August 2001

Nonoxidative glucose consumption during focal physiologic neural activity
journal, July 1988

Cocaine-Induced Redoppuction of Glucose Utilization in Human Brain: A Study Using Positron Emission Tomography and [Fluorine 18]-Fluorodeoxyglucose
journal, June 1990

Brain work and Brain Imaging
journal, July 2006

Dynamic models of BOLD contrast
journal, August 2012

Effects of Chronic Cocaine Self-Administration on Cognition and Cerebral Glucose Utilization in Rhesus Monkeys
journal, November 2012

Neurovascular coupling to D2/D3 dopamine receptor occupancy using simultaneous PET/functional MRI
journal, May 2013

Influence of Plasma Glucose Concentration on Lumped Constant of the Deoxyglucose Method: Effects of Hyperglycemia in the Rat
journal, November 1990

Translational MR Neuroimaging of Stroke and Recovery
journal, August 2016

MR-PET head motion correction based on co-registration of multi-contrast MR images
posted_content, January 2018

DREAMM: A Biobehavioral Imaging Methodology for Dynamic In Vivo Whole-Brain Mapping of Cell Type-Specific Functional Networks
journal, December 2014

Combined PET/MRI: from Status Quo to Status Go. Summary Report of the Fifth International Workshop on PET/MR Imaging; February 15–19, 2016; Tübingen, Germany
journal, August 2016

Functional dynamics of dopamine synthesis during monetary reward and punishment processing
posted_content, December 2020

From simultaneous to synergistic MR‐PET brain imaging: A review of hybrid MR‐PET imaging methodologies
journal, August 2018

Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus
journal, September 2019

Functional dynamics of dopamine synthesis during monetary reward and punishment processing
journal, May 2021

Simultaneous EEG–PET–fMRI measurements in disorders of consciousness: an exploratory study on diagnosis and prognosis
journal, August 2017

Constant Infusion Radiotracer Administration for High Temporal Resolution Positron Emission Tomography (PET) of the Human Brain: Application to [18F]-Fluorodexoyglucose PET (FDG-PET)
posted_content, June 2019

Analysis of continuous infusion functional PET (fPET) in the human brain
journal, June 2020

Effects of flow changes on radiotracer binding: Simultaneous measurement of neuroreceptor binding and cerebral blood flow modulation
journal, August 2017

Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex
posted_content, October 2018

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images?
journal, September 2017

The renaissance of functional 18F-FDG PET brain activation imaging
journal, September 2018

Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex
journal, April 2019

Imaging mitochondrial complex I activation during a vibrotactile stimulation: A PET study using [ ¹⁸ F]BCPP-EF in the conscious monkey brain
journal, January 2020

Inflammation in Post-Traumatic Stress Disorder (PTSD): A Review of Potential Correlates of PTSD with a Neurological Perspective
journal, January 2020

Evaluation of Task-Related Brain Activity: Is There a Role for ¹⁸ F FDG-PET Imaging?
journal, July 2019

MR-PET head motion correction based on co-registration of multicontrast MR images
journal, January 2019

Analysis of continuous infusion functional PET (fPET) in the human brain
posted_content, September 2019

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images?
text, January 2017

Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI
posted_content, January 2019

Metabolite concentration changes associated with positive and negative BOLD responses in the human visual cortex: A functional MRS study at 7 Tesla
journal, February 2019

Simultaneous PET-MRI imaging of cerebral blood flow and glucose metabolism in the symptomatic unilateral internal carotid artery/middle cerebral artery steno-occlusive disease
journal, November 2019

Dynamic coupling between fMRI local connectivity and interictal EEG in focal epilepsy: A wavelet analysis approach: Dynamic Coupling between fMRI Local Connectivity and Interictal EEG in Focal Epilepsy
journal, July 2017

Structure of the Human 4-Hydroxyphenylpyruvic Acid Dioxygenase Gene (HPD)
journal, October 1994

Task-relevant brain networks identified with simultaneous PET/MR imaging of metabolism and connectivity
journal, November 2017

Combined PET/MRI: from Status Quo to Status Go. Summary Report of the Fifth International Workshop on PET/MR Imaging; February 15–19, 2016; Tübingen, Germany
journal, August 2016

MR-PET head motion correction based on co-registration of multi-contrast MR images
posted_content, January 2018

Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images?
text, January 2017

The Effects of Capillary Transit Time Heterogeneity (CTH) on the Cerebral Uptake of Glucose and Glucose Analogs: Application to FDG and Comparison to Oxygen Uptake
journal, October 2016

Inflammation in Post-Traumatic Stress Disorder (PTSD): A Review of Potential Correlates of PTSD with a Neurological Perspective
journal, January 2020