Quantitative and simultaneous measurement of oxygen consumption rates in rat brain and skeletal muscle using 17O MRS imaging at 16.4T

Hannes M. Wiesner; Dávid Z. Balla; Klaus Scheffler; Kâmil Uğurbil; Xiao Hong Zhu; Wei Chen; Kâmil Uludağ; Rolf Pohmann

doi:10.1002/mrm.28552

Quantitative and simultaneous measurement of oxygen consumption rates in rat brain and skeletal muscle using ¹⁷O MRS imaging at 16.4T

Hannes M. Wiesner, Dávid Z. Balla, Klaus Scheffler, Kâmil Uğurbil, Xiao Hong Zhu, Wei Chen, Kâmil Uludağ, Rolf Pohmann

Center for Magnetic Resonance Research

Research output: Contribution to journal › Article › peer-review

11 Scopus citations

Abstract

Purpose: Oxygen-17 (¹⁷O) MRS imaging, successfully used in the brain, is extended by imaging the oxygen metabolic rate in the resting skeletal muscle and used to determine the total whole-body oxygen metabolic rate in the rat. Methods: During and after inhalations of ¹⁷O₂ gas, dynamic ¹⁷O MRSI was performed in rats (n = 8) ventilated with N₂O or N₂ at 16.4 T. Time courses of the H₂¹⁷O concentration from regions of interest located in brain and muscle tissue were examined and used to fit an animal-adapted 3-phase metabolic model of oxygen consumption. CBF was determined with an independent washout method. Finally, body oxygen metabolic rate was calculated using a global steady-state approach. Results: Cerebral metabolic rate of oxygen consumption was 1.97 ± 0.19 μmol/g/min on average. The resting metabolic rate of oxygen consumption in skeletal muscle was 0.32 ± 0.12 μmol/g/min and >6 times lower than cerebral metabolic rate of oxygen consumption. Global oxygen consumed by the body was 24.2 ± 3.6 mL O₂/kg body weight/min. CBF was estimated to be 0.28 ± 0.02 mL/g/min and 0.34 ± 0.06 mL/g/min for the N₂ and N₂O ventilation condition, respectively. Conclusion: We have evaluated the feasibility of ¹⁷O MRSI for imaging and quantifying the oxygen consumption rate in low metabolizing organs such as the skeletal muscle at rest. Additionally, we have shown that CBF is slightly increased in the case of ventilation with N₂O. We expect this study to be beneficial to the application of ¹⁷O MRSI to a wider range of organs, although further validation is advised.

Original language	English (US)
Pages (from-to)	2232-2246
Number of pages	15
Journal	Magnetic resonance in medicine
Volume	85
Issue number	4
DOIs	https://doi.org/10.1002/mrm.28552
State	Published - Oct 26 2020

Bibliographical note

Funding Information:
The study was sponsored by the Max Planck Society and in part by the NIH grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061 and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to Kâmil Uludağ. Open access funding enabled and organized by Projekt DEAL.

Funding Information:
The study was sponsored by the Max Planck Society and in part by the National Institutes of Health (NIH) grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061; and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to Kâmil Uludağ

Publisher Copyright:
© 2020 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine

Keywords

O MRSI of HO
cerebral blood flow (CBF)
cerebral metabolic rate of oxygen (CMRO)
mitochondrial water
muscle resting metabolic rate of oxygen consumption
skeletal muscle metabolism
total body oxygen consumption (VO)

Center for Magnetic Resonance Research (CMRR) tags

BEMIT
MRE
P41

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10.1002/mrm.28552

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@article{6bc3d728f8314b9c98e12b5a7bcce076,

title = "Quantitative and simultaneous measurement of oxygen consumption rates in rat brain and skeletal muscle using 17O MRS imaging at 16.4T",

abstract = "Purpose: Oxygen-17 (17O) MRS imaging, successfully used in the brain, is extended by imaging the oxygen metabolic rate in the resting skeletal muscle and used to determine the total whole-body oxygen metabolic rate in the rat. Methods: During and after inhalations of 17O2 gas, dynamic 17O MRSI was performed in rats (n = 8) ventilated with N2O or N2 at 16.4 T. Time courses of the H217O concentration from regions of interest located in brain and muscle tissue were examined and used to fit an animal-adapted 3-phase metabolic model of oxygen consumption. CBF was determined with an independent washout method. Finally, body oxygen metabolic rate was calculated using a global steady-state approach. Results: Cerebral metabolic rate of oxygen consumption was 1.97 ± 0.19 μmol/g/min on average. The resting metabolic rate of oxygen consumption in skeletal muscle was 0.32 ± 0.12 μmol/g/min and >6 times lower than cerebral metabolic rate of oxygen consumption. Global oxygen consumed by the body was 24.2 ± 3.6 mL O2/kg body weight/min. CBF was estimated to be 0.28 ± 0.02 mL/g/min and 0.34 ± 0.06 mL/g/min for the N2 and N2O ventilation condition, respectively. Conclusion: We have evaluated the feasibility of 17O MRSI for imaging and quantifying the oxygen consumption rate in low metabolizing organs such as the skeletal muscle at rest. Additionally, we have shown that CBF is slightly increased in the case of ventilation with N2O. We expect this study to be beneficial to the application of 17O MRSI to a wider range of organs, although further validation is advised.",

keywords = "O MRSI of HO, cerebral blood flow (CBF), cerebral metabolic rate of oxygen (CMRO), mitochondrial water, muscle resting metabolic rate of oxygen consumption, skeletal muscle metabolism, total body oxygen consumption (VO)",

author = "Wiesner, {Hannes M.} and Balla, {D{\'a}vid Z.} and Klaus Scheffler and K{\^a}mil Uğurbil and Zhu, {Xiao Hong} and Wei Chen and K{\^a}mil Uludağ and Rolf Pohmann",

note = "Funding Information: The study was sponsored by the Max Planck Society and in part by the NIH grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061 and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to K{\^a}mil Uludağ. Open access funding enabled and organized by Projekt DEAL. Funding Information: The study was sponsored by the Max Planck Society and in part by the National Institutes of Health (NIH) grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061; and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to K{\^a}mil Uludağ Publisher Copyright: {\textcopyright} 2020 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine",

year = "2020",

month = oct,

day = "26",

doi = "10.1002/mrm.28552",

language = "English (US)",

volume = "85",

pages = "2232--2246",

journal = "Magnetic resonance in medicine",

issn = "0740-3194",

publisher = "John Wiley and Sons Inc.",

number = "4",

}

TY - JOUR

T1 - Quantitative and simultaneous measurement of oxygen consumption rates in rat brain and skeletal muscle using 17O MRS imaging at 16.4T

AU - Wiesner, Hannes M.

AU - Balla, Dávid Z.

AU - Scheffler, Klaus

AU - Uğurbil, Kâmil

AU - Zhu, Xiao Hong

AU - Chen, Wei

AU - Uludağ, Kâmil

AU - Pohmann, Rolf

N1 - Funding Information: The study was sponsored by the Max Planck Society and in part by the NIH grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061 and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to Kâmil Uludağ. Open access funding enabled and organized by Projekt DEAL. Funding Information: The study was sponsored by the Max Planck Society and in part by the National Institutes of Health (NIH) grants: R01 NS070839, R01 MH111413, R01 CA240953, U01 EB026978, and P41 EB027061; and by the Institute for Basic Science, Suwon, Republic of South Korea (IBS‐R015‐D1) to Kâmil Uludağ Publisher Copyright: © 2020 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine

PY - 2020/10/26

Y1 - 2020/10/26

N2 - Purpose: Oxygen-17 (17O) MRS imaging, successfully used in the brain, is extended by imaging the oxygen metabolic rate in the resting skeletal muscle and used to determine the total whole-body oxygen metabolic rate in the rat. Methods: During and after inhalations of 17O2 gas, dynamic 17O MRSI was performed in rats (n = 8) ventilated with N2O or N2 at 16.4 T. Time courses of the H217O concentration from regions of interest located in brain and muscle tissue were examined and used to fit an animal-adapted 3-phase metabolic model of oxygen consumption. CBF was determined with an independent washout method. Finally, body oxygen metabolic rate was calculated using a global steady-state approach. Results: Cerebral metabolic rate of oxygen consumption was 1.97 ± 0.19 μmol/g/min on average. The resting metabolic rate of oxygen consumption in skeletal muscle was 0.32 ± 0.12 μmol/g/min and >6 times lower than cerebral metabolic rate of oxygen consumption. Global oxygen consumed by the body was 24.2 ± 3.6 mL O2/kg body weight/min. CBF was estimated to be 0.28 ± 0.02 mL/g/min and 0.34 ± 0.06 mL/g/min for the N2 and N2O ventilation condition, respectively. Conclusion: We have evaluated the feasibility of 17O MRSI for imaging and quantifying the oxygen consumption rate in low metabolizing organs such as the skeletal muscle at rest. Additionally, we have shown that CBF is slightly increased in the case of ventilation with N2O. We expect this study to be beneficial to the application of 17O MRSI to a wider range of organs, although further validation is advised.

AB - Purpose: Oxygen-17 (17O) MRS imaging, successfully used in the brain, is extended by imaging the oxygen metabolic rate in the resting skeletal muscle and used to determine the total whole-body oxygen metabolic rate in the rat. Methods: During and after inhalations of 17O2 gas, dynamic 17O MRSI was performed in rats (n = 8) ventilated with N2O or N2 at 16.4 T. Time courses of the H217O concentration from regions of interest located in brain and muscle tissue were examined and used to fit an animal-adapted 3-phase metabolic model of oxygen consumption. CBF was determined with an independent washout method. Finally, body oxygen metabolic rate was calculated using a global steady-state approach. Results: Cerebral metabolic rate of oxygen consumption was 1.97 ± 0.19 μmol/g/min on average. The resting metabolic rate of oxygen consumption in skeletal muscle was 0.32 ± 0.12 μmol/g/min and >6 times lower than cerebral metabolic rate of oxygen consumption. Global oxygen consumed by the body was 24.2 ± 3.6 mL O2/kg body weight/min. CBF was estimated to be 0.28 ± 0.02 mL/g/min and 0.34 ± 0.06 mL/g/min for the N2 and N2O ventilation condition, respectively. Conclusion: We have evaluated the feasibility of 17O MRSI for imaging and quantifying the oxygen consumption rate in low metabolizing organs such as the skeletal muscle at rest. Additionally, we have shown that CBF is slightly increased in the case of ventilation with N2O. We expect this study to be beneficial to the application of 17O MRSI to a wider range of organs, although further validation is advised.

KW - O MRSI of HO

KW - cerebral blood flow (CBF)

KW - cerebral metabolic rate of oxygen (CMRO)

KW - mitochondrial water

KW - muscle resting metabolic rate of oxygen consumption

KW - skeletal muscle metabolism

KW - total body oxygen consumption (VO)

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U2 - 10.1002/mrm.28552

DO - 10.1002/mrm.28552

M3 - Article

C2 - 33104248

AN - SCOPUS:85093697301

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VL - 85

SP - 2232

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JO - Magnetic resonance in medicine

JF - Magnetic resonance in medicine

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