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Published in: Journal of Inflammation 1/2016

Open Access 01-12-2016 | Research

Interleukin-1beta-induced reduction of tissue water diffusion in the juvenile rat brain on ADC MRI is not associated with 31P MRS-detectable energy failure

Author: Raman Saggu

Published in: Journal of Inflammation | Issue 1/2016

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Abstract

Background

It has long been known that an intrastriatal microinjection of the archetypal pro-inflammatory cytokine, interleukin-1beta (IL-1β), in juvenile rats induces a chronic reduction in the apparent diffusion coefficient (ADC) of tissue water on magnetic resonance imaging (MRI). Reduced ADC during acute cerebral ischaemia is an established indicator of metabolic failure whereas the cause of the IL-1β-induced reduction remains to be deciphered. Previously, it has been shown that IL-1β does not perturb the phosphorus (31P) magnetic resonance spectroscopy (MRS)-detectable energy status of an ex vivo preparation of rat brain parenchyma that is devoid of a functional vasculature component. However, brain energy status following an IL-1β challenge in vivo remains to be examined.

Methods

This study is the first longitudinal in vivo examination of the correlation of ADC MRI with localised 31P MRS signals obtained specifically from within the injected and non-injected striatum following IL-1β (1 ng/ul or 100 ng/ul) challenge, in real-time.

Results

Despite observing a chronic reduction in ADC at either dose of IL-1β challenge, energy compromise was not detected at any time point.

Conclusions

The IL-1β-induced effects pertaining to a functional vasculature such as leukocyte recruitment, blood–brain barrier (BBB) breakdown and blood flow changes are unlikely to impact on overall tissue energy status. Compared to classic ischaemia, there is dissociation between ADC and energy status within an IL-1β-induced lesion in vivo.
Literature
1.
2.
go back to reference Leal MC et al. Interleukin-1beta and tumor necrosis factor-alpha: reliable targets for protective therapies in Parkinson’s Disease? Front Cell Neurosci. 2013;7:53.CrossRefPubMedPubMedCentral Leal MC et al. Interleukin-1beta and tumor necrosis factor-alpha: reliable targets for protective therapies in Parkinson’s Disease? Front Cell Neurosci. 2013;7:53.CrossRefPubMedPubMedCentral
3.
go back to reference Blamire AM et al. Interleukin-1beta -induced changes in blood–brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J Neurosci. 2000;20(21):8153–9.PubMed Blamire AM et al. Interleukin-1beta -induced changes in blood–brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J Neurosci. 2000;20(21):8153–9.PubMed
4.
go back to reference Moseley ME et al. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med. 1990;14(2):330–46.CrossRefPubMed Moseley ME et al. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med. 1990;14(2):330–46.CrossRefPubMed
5.
go back to reference Busza AL et al. Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke. 1992;23(11):1602–12.CrossRefPubMed Busza AL et al. Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke. 1992;23(11):1602–12.CrossRefPubMed
6.
go back to reference Back T et al. Diffusion nuclear magnetic resonance imaging in experimental stroke. Correlation with cerebral metabolites. Stroke. 1994;25(2):494–500.CrossRefPubMed Back T et al. Diffusion nuclear magnetic resonance imaging in experimental stroke. Correlation with cerebral metabolites. Stroke. 1994;25(2):494–500.CrossRefPubMed
7.
go back to reference Astrup J. Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg. 1982;56(4):482–97.CrossRefPubMed Astrup J. Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg. 1982;56(4):482–97.CrossRefPubMed
8.
go back to reference Hansen AJ, Olsen CE. Brain extracellular space during spreading depression and ischemia. Acta Physiol Scand. 1980;108(4):355–65.CrossRefPubMed Hansen AJ, Olsen CE. Brain extracellular space during spreading depression and ischemia. Acta Physiol Scand. 1980;108(4):355–65.CrossRefPubMed
9.
go back to reference Kohno K et al. Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging. 1995;13(1):73–80.CrossRefPubMed Kohno K et al. Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging. 1995;13(1):73–80.CrossRefPubMed
10.
go back to reference Verheul HB et al. Comparison of diffusion-weighted MRI with changes in cell volume in a rat model of brain injury. NMR Biomed. 1994;7(1–2):96–100.CrossRefPubMed Verheul HB et al. Comparison of diffusion-weighted MRI with changes in cell volume in a rat model of brain injury. NMR Biomed. 1994;7(1–2):96–100.CrossRefPubMed
11.
go back to reference Mintorovitch J et al. Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn Reson Med. 1991;18(1):39–50.CrossRefPubMed Mintorovitch J et al. Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn Reson Med. 1991;18(1):39–50.CrossRefPubMed
12.
go back to reference Anthony DC et al. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood–brain barrier permeability in rats. Brain. 1997;120(Pt 3):435–44.CrossRefPubMed Anthony DC et al. Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood–brain barrier permeability in rats. Brain. 1997;120(Pt 3):435–44.CrossRefPubMed
13.
go back to reference Anthony D et al. CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood–brain barrier breakdown. Curr Biol. 1998;8(16):923–6.CrossRefPubMed Anthony D et al. CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood–brain barrier breakdown. Curr Biol. 1998;8(16):923–6.CrossRefPubMed
14.
go back to reference Dijkhuizen RM et al. Status of the neonatal rat brain after NMDA-induced excitotoxic injury as measured by MRI, MRS and metabolic imaging. NMR Biomed. 1996;9(2):84–92.CrossRefPubMed Dijkhuizen RM et al. Status of the neonatal rat brain after NMDA-induced excitotoxic injury as measured by MRI, MRS and metabolic imaging. NMR Biomed. 1996;9(2):84–92.CrossRefPubMed
15.
go back to reference Veldhuis WB et al. In vivo excitotoxicity induced by ouabain, a Na+/K + −ATPase inhibitor. J Cereb Blood Flow Metab. 2003;23(1):62–74.CrossRefPubMed Veldhuis WB et al. In vivo excitotoxicity induced by ouabain, a Na+/K + −ATPase inhibitor. J Cereb Blood Flow Metab. 2003;23(1):62–74.CrossRefPubMed
16.
go back to reference Zhong J et al. Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus. Magn Reson Med. 1993;30(2):241–6.CrossRefPubMed Zhong J et al. Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus. Magn Reson Med. 1993;30(2):241–6.CrossRefPubMed
17.
go back to reference Saggu R et al. Interleukin-1beta does not affect the energy metabolism of rat organotypic hippocampal-slice cultures. Neurosci Lett. 2012;508(2):114–8.CrossRefPubMed Saggu R et al. Interleukin-1beta does not affect the energy metabolism of rat organotypic hippocampal-slice cultures. Neurosci Lett. 2012;508(2):114–8.CrossRefPubMed
18.
go back to reference Hochachka PW et al. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proc Natl Acad Sci U S A. 1996;93(3):1215–20.CrossRefPubMedPubMedCentral Hochachka PW et al. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proc Natl Acad Sci U S A. 1996;93(3):1215–20.CrossRefPubMedPubMedCentral
19.
go back to reference Stejskal EO, Tanner JE. Spin diffusion measurements: Spin echoes in the presence of a time-dependent field gradient. J Chem Phys. 1963;42:288–92.CrossRef Stejskal EO, Tanner JE. Spin diffusion measurements: Spin echoes in the presence of a time-dependent field gradient. J Chem Phys. 1963;42:288–92.CrossRef
20.
go back to reference Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B. 1994;103(3):247–54.CrossRefPubMed Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B. 1994;103(3):247–54.CrossRefPubMed
21.
go back to reference Ordidge RJ et al. Correction of motional artifacts in diffusion-weighted MR images using navigator echoes. Magn Reson Imaging. 1994;12(3):455–60.CrossRefPubMed Ordidge RJ et al. Correction of motional artifacts in diffusion-weighted MR images using navigator echoes. Magn Reson Imaging. 1994;12(3):455–60.CrossRefPubMed
22.
23.
go back to reference Le Fur Y et al. Grid-free interactive and automated data processing for MR chemical shift imaging data. MAGMA. 2010;23(1):23–30.CrossRefPubMed Le Fur Y et al. Grid-free interactive and automated data processing for MR chemical shift imaging data. MAGMA. 2010;23(1):23–30.CrossRefPubMed
24.
go back to reference Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997;129(1):35–43.CrossRefPubMed Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997;129(1):35–43.CrossRefPubMed
25.
go back to reference Rosner B. Sample-size Estimation for Longitudinal Studies, in Fundamentals of Biostatistics. Boston: Brooks/Cole; 2011. p. 305. Rosner B. Sample-size Estimation for Longitudinal Studies, in Fundamentals of Biostatistics. Boston: Brooks/Cole; 2011. p. 305.
26.
go back to reference Shoubridge EA, Briggs RW, Radda GK. 31p NMR saturation transfer measurements of the steady state rates of creatine kinase and ATP synthetase in the rat brain. FEBS Lett. 1982;140(2):289–92.CrossRefPubMed Shoubridge EA, Briggs RW, Radda GK. 31p NMR saturation transfer measurements of the steady state rates of creatine kinase and ATP synthetase in the rat brain. FEBS Lett. 1982;140(2):289–92.CrossRefPubMed
27.
go back to reference Horikawa Y et al. In vivo studies of energy metabolism in experimental cerebral ischemia using topical magnetic resonance. Changes in 31P-nuclear magnetic resonance spectra compared with electroencephalograms and regional cerebral blood flow. J Cereb Blood Flow Metab. 1985;5(2):235–40.CrossRefPubMed Horikawa Y et al. In vivo studies of energy metabolism in experimental cerebral ischemia using topical magnetic resonance. Changes in 31P-nuclear magnetic resonance spectra compared with electroencephalograms and regional cerebral blood flow. J Cereb Blood Flow Metab. 1985;5(2):235–40.CrossRefPubMed
28.
go back to reference Naruse S et al. In vivo measurement of energy metabolism and the concomitant monitoring of electroencephalogram in experimental cerebral ischemia. Brain Res. 1984;296(2):370–2.CrossRefPubMed Naruse S et al. In vivo measurement of energy metabolism and the concomitant monitoring of electroencephalogram in experimental cerebral ischemia. Brain Res. 1984;296(2):370–2.CrossRefPubMed
29.
go back to reference Naruse S et al. In vivo 31P NMR studies on experimental cerebral infarction. Jpn J Physiol. 1983;33(1):19–28.CrossRefPubMed Naruse S et al. In vivo 31P NMR studies on experimental cerebral infarction. Jpn J Physiol. 1983;33(1):19–28.CrossRefPubMed
30.
go back to reference Bolas NM et al. Metabolic changes during experimental cerebral ischemia in hyperglycemic rats, observed by 31P and 1H magnetic resonance spectroscopy. Stroke. 1988;19(5):608–14.CrossRefPubMed Bolas NM et al. Metabolic changes during experimental cerebral ischemia in hyperglycemic rats, observed by 31P and 1H magnetic resonance spectroscopy. Stroke. 1988;19(5):608–14.CrossRefPubMed
31.
go back to reference Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke. 1992;23(5):746–54.CrossRefPubMed Benveniste H, Hedlund LW, Johnson GA. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke. 1992;23(5):746–54.CrossRefPubMed
32.
go back to reference Hanstock CC et al. Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke. 1994;25(4):843–8.CrossRefPubMed Hanstock CC et al. Diffusion-weighted imaging differentiates ischemic tissue from traumatized tissue. Stroke. 1994;25(4):843–8.CrossRefPubMed
33.
go back to reference Hoehn-Berlage M et al. Changes of relaxation times (T1, T2) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology. Magn Reson Med. 1995;34(6):824–34.CrossRefPubMed Hoehn-Berlage M et al. Changes of relaxation times (T1, T2) and apparent diffusion coefficient after permanent middle cerebral artery occlusion in the rat: temporal evolution, regional extent, and comparison with histology. Magn Reson Med. 1995;34(6):824–34.CrossRefPubMed
34.
go back to reference Hossmann KA et al. NMR imaging of the apparent diffusion coefficient (ADC) for the evaluation of metabolic suppression and recovery after prolonged cerebral ischemia. J Cereb Blood Flow Metab. 1994;14(5):723–31.CrossRefPubMed Hossmann KA et al. NMR imaging of the apparent diffusion coefficient (ADC) for the evaluation of metabolic suppression and recovery after prolonged cerebral ischemia. J Cereb Blood Flow Metab. 1994;14(5):723–31.CrossRefPubMed
35.
go back to reference Swanson RA, Choi DW. Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab. 1993;13(1):162–9.CrossRefPubMed Swanson RA, Choi DW. Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab. 1993;13(1):162–9.CrossRefPubMed
36.
go back to reference Gavillet M, Allaman I, Magistretti PJ. Modulation of astrocytic metabolic phenotype by proinflammatory cytokines. Glia. 2008;56(9):975–89.CrossRefPubMed Gavillet M, Allaman I, Magistretti PJ. Modulation of astrocytic metabolic phenotype by proinflammatory cytokines. Glia. 2008;56(9):975–89.CrossRefPubMed
37.
go back to reference Belanger M, Allaman I, Magistretti PJ. Differential effects of pro- and anti-inflammatory cytokines alone or in combinations on the metabolic profile of astrocytes. J Neurochem. 2011;116(4):564–76.CrossRefPubMed Belanger M, Allaman I, Magistretti PJ. Differential effects of pro- and anti-inflammatory cytokines alone or in combinations on the metabolic profile of astrocytes. J Neurochem. 2011;116(4):564–76.CrossRefPubMed
38.
go back to reference Kitamura S et al. Longitudinal white matter changes in Alzheimer’s disease: a tractography-based analysis study. Brain Res. 2013;1515:12–8.CrossRefPubMed Kitamura S et al. Longitudinal white matter changes in Alzheimer’s disease: a tractography-based analysis study. Brain Res. 2013;1515:12–8.CrossRefPubMed
39.
go back to reference Zimny A et al. Quantitative MR evaluation of atrophy, as well as perfusion and diffusion alterations within hippocampi in patients with Alzheimer’s disease and mild cognitive impairment. Med Sci Monit. 2013;19:86–94.CrossRefPubMedPubMedCentral Zimny A et al. Quantitative MR evaluation of atrophy, as well as perfusion and diffusion alterations within hippocampi in patients with Alzheimer’s disease and mild cognitive impairment. Med Sci Monit. 2013;19:86–94.CrossRefPubMedPubMedCentral
40.
go back to reference Schwarz ST et al. Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: A region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin. 2013;3:481–8.CrossRefPubMedPubMedCentral Schwarz ST et al. Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: A region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin. 2013;3:481–8.CrossRefPubMedPubMedCentral
Metadata
Title
Interleukin-1beta-induced reduction of tissue water diffusion in the juvenile rat brain on ADC MRI is not associated with 31P MRS-detectable energy failure
Author
Raman Saggu
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Inflammation / Issue 1/2016
Electronic ISSN: 1476-9255
DOI
https://doi.org/10.1186/s12950-016-0118-3

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