Using a Multimodal Near-infrared Spectroscopy and MRI to Quantify Gray Matter Metabolic Rate for Oxygen: A Hypothermia Validation Study

Overview

Journal Neuroimage

Specialty Radiology

Date 2019 Nov 1

PMID 31669409

Citations 13

Authors

Mada Hashem

Qiong Zhang

Ying Wu

Thomas W Johnson

Jeff F Dunn

Affiliations

Soon will be listed here.

Abstract

Non-invasive quantitative imaging of cerebral oxygen metabolism (CMRO) in small animal models is crucial to understand the role of oxidative metabolism in healthy and diseased brains. In this study, we developed a multimodal method combining near-infrared spectroscopy (NIRS) and MRI to non-invasively study oxygen delivery and consumption in the cortex of mouse and rat models. The term CASNIRS is proposed to the technique that measures CMRO with ASL and NIRS. To determine the reliability of this method, CMRO values were compared with reported values measured with other techniques. Also, the sensitivity of the CASNIRS technique to detect changes in CMRO in the cortex of the animals was assessed by applying a reduction in core temperature, which is known to reduce CMRO. Cerebral blood flow (CBF) and CMRO were measured in five mice and five rats at a core temperature of 37 °C followed by another measurement at 33 °C. CMRO was 7.8 ± 1.8 and 3.7 ± 0.9 (ml/100 g/min, mean ± SD) in mice and rats respectively. These values are in good agreement with reported values measured by O PET, O NMR, and BOLD fMRI. In hypothermia, we detected a significant decrease of 37% and 32% in CMRO in the cortex of mice and rats, respectively. Q10 was calculated to be 3.2 in mice and 2.7 in rats. In this study we showed that it is possible to assess absolute values of metabolic correlates such as CMRO, CBF and oxygen extraction fraction (OEF) noninvasively in living brain of mice and rats by combining NIRS with MRI. This will open new possibilities for studying brain metabolism in patients as well as the many mouse/rat models of brain disorders.

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References

Yang R, Dunn J . Reduced cortical microvascular oxygenation in multiple sclerosis: a blinded, case-controlled study using a novel quantitative near-infrared spectroscopy method. Sci Rep. 2015; 5:16477. PMC: 4643232. DOI: 10.1038/srep16477. View

Hyder F, Kida I, Behar K, Kennan R, Maciejewski P, Rothman D . Quantitative functional imaging of the brain: towards mapping neuronal activity by BOLD fMRI. NMR Biomed. 2001; 14(7-8):413-31. DOI: 10.1002/nbm.733. View

Buxton R . Quantifying CBF with arterial spin labeling. J Magn Reson Imaging. 2005; 22(6):723-6. DOI: 10.1002/jmri.20462. View

Lou S, Lepak V, Eberly L, Roth B, Cui W, Zhu X . Oxygen consumption deficit in Huntington disease mouse brain under metabolic stress. Hum Mol Genet. 2016; 25(13):2813-2826. PMC: 5181641. DOI: 10.1093/hmg/ddw138. View

Mintun M, Raichle M, Martin W, Herscovitch P . Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J Nucl Med. 1984; 25(2):177-87. View

Temma T, Yamazaki M, Miyanohara J, Shirakawa H, Kondo N, Koshino K . Sequential PET estimation of cerebral oxygen metabolism with spontaneous respiration of O-gas in mice with bilateral common carotid artery stenosis. J Cereb Blood Flow Metab. 2017; 37(10):3334-3343. PMC: 5624393. DOI: 10.1177/0271678X17692815. View

Lin M, Beal M . Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006; 443(7113):787-95. DOI: 10.1038/nature05292. View

Zhu X, Zhang Y, Zhang N, Ugurbil K, Chen W . Noninvasive and three-dimensional imaging of CMRO(2) in rats at 9.4 T: reproducibility test and normothermia/hypothermia comparison study. J Cereb Blood Flow Metab. 2006; 27(6):1225-34. DOI: 10.1038/sj.jcbfm.9600421. View

Tichauer K, Brown D, Hadway J, Lee T, St Lawrence K . Near-infrared spectroscopy measurements of cerebral blood flow and oxygen consumption following hypoxia-ischemia in newborn piglets. J Appl Physiol (1985). 2005; 100(3):850-7. DOI: 10.1152/japplphysiol.00830.2005. View

10.

Zhu X, Zhang N, Zhang Y, Zhang X, Ugurbil K, Chen W . In vivo 17O NMR approaches for brain study at high field. NMR Biomed. 2005; 18(2):83-103. DOI: 10.1002/nbm.930. View

11.

Klementavicius R, Nemoto E, Yonas H . The Q10 ratio for basal cerebral metabolic rate for oxygen in rats. J Neurosurg. 1996; 85(3):482-7. DOI: 10.3171/jns.1996.85.3.0482. View

12.

Sicard K, Duong T . Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. Neuroimage. 2005; 25(3):850-8. PMC: 2962945. DOI: 10.1016/j.neuroimage.2004.12.010. View

13.

Ching S, Purdon P, Vijayan S, Kopell N, Brown E . A neurophysiological-metabolic model for burst suppression. Proc Natl Acad Sci U S A. 2012; 109(8):3095-100. PMC: 3286963. DOI: 10.1073/pnas.1121461109. View

14.

Phelps M, Huang S, Hoffman E, Kuhl D . Validation of tomographic measurement of cerebral blood volume with C-11-labeled carboxyhemoglobin. J Nucl Med. 1979; 20(4):328-34. View

15.

Chuang C, Chen C, Hsieh Y, Liu T, Sun C . Brain structure and spatial sensitivity profile assessing by near-infrared spectroscopy modeling based on 3D MRI data. J Biophotonics. 2012; 6(3):267-74. DOI: 10.1002/jbio.201200025. View

16.

Shiozaki T, Sugimoto H, Taneda M, Yoshida H, Iwai A, Yoshioka T . Effect of mild hypothermia on uncontrollable intracranial hypertension after severe head injury. J Neurosurg. 1993; 79(3):363-8. DOI: 10.3171/jns.1993.79.3.0363. View

17.

Yee S, Lee K, Jerabek P, Fox P . Quantitative measurement of oxygen metabolic rate in the rat brain using microPET imaging of briefly inhaled 15O-labelled oxygen gas. Nucl Med Commun. 2006; 27(7):573-81. DOI: 10.1097/01.mnm.0000220586.02591.fd. View

18.

Ni R, Rudin M, Klohs J . Cortical hypoperfusion and reduced cerebral metabolic rate of oxygen in the arcAβ mouse model of Alzheimer's disease. Photoacoustics. 2018; 10:38-47. PMC: 5909030. DOI: 10.1016/j.pacs.2018.04.001. View

19.

Michenfelder J, Milde J . The relationship among canine brain temperature, metabolism, and function during hypothermia. Anesthesiology. 1991; 75(1):130-6. DOI: 10.1097/00000542-199107000-00021. View

20.

Herscovitch P, Raichle M . What is the correct value for the brain--blood partition coefficient for water?. J Cereb Blood Flow Metab. 1985; 5(1):65-9. DOI: 10.1038/jcbfm.1985.9. View