A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity

Abstract While the dire cardiometabolic consequences of the hypercaloric modern ‘Western’ diet are well known, there is not much information on the health impact of a high sucrose diet not inducing weight gain. Here, we tested the hypothesis that rats reared with intermittent binge access to sucrose...

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Main Authors: Omkar L. Patkar, Abdalla Z. Mohamed, Ashwin Narayanan, Karine Mardon, Gary Cowin, Rajiv Bhalla, Damion H. R. Stimson, Michael Kassiou, Kate Beecher, Arnauld Belmer, Ignatius Alvarez Cooper, Michael Morgan, David A. Hume, Katharine M. Irvine, Selena E. Bartlett, Fatima Nasrallah, Paul Cumming
Format: Article
Language:English
Published: Nature Publishing Group 2021-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-90817-z
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spelling doaj-c523c0f955e34761879d7926be4d415f2021-05-30T11:35:55ZengNature Publishing GroupScientific Reports2045-23222021-05-0111111110.1038/s41598-021-90817-zA binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesityOmkar L. Patkar0Abdalla Z. Mohamed1Ashwin Narayanan2Karine Mardon3Gary Cowin4Rajiv Bhalla5Damion H. R. Stimson6Michael Kassiou7Kate Beecher8Arnauld Belmer9Ignatius Alvarez Cooper10Michael Morgan11David A. Hume12Katharine M. Irvine13Selena E. Bartlett14Fatima Nasrallah15Paul Cumming16Macrophage Biology Group, Mater Research, Translational Research InstituteQueensland Brain Institute, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandSchool of Chemistry, University of SydneyQueensland University of Technology, Translational Research InstituteQueensland University of Technology, Translational Research InstituteQueensland University of Technology, Translational Research InstituteDepartment of Anatomy and Neuroscience, The University of MelbourneMacrophage Biology Group, Mater Research, Translational Research InstituteMacrophage Biology Group, Mater Research, Translational Research InstituteQueensland University of Technology, Translational Research InstituteQueensland Brain Institute, The University of QueenslandDepartment of Nuclear Medicine, Inselspital, Bern UniversityAbstract While the dire cardiometabolic consequences of the hypercaloric modern ‘Western’ diet are well known, there is not much information on the health impact of a high sucrose diet not inducing weight gain. Here, we tested the hypothesis that rats reared with intermittent binge access to sucrose in addition to normal chow would develop an inflammatory response in brain. To test this hypothesis, we undertook serial PET/MRI scans with the TSPO ligand [18F]DPA714 in a group of (n=9) rats at baseline and again after voluntarily consuming 5% sucrose solution three days a week for three months. Compared to a control group fed with normal chow (n=9), the sucrose rats indeed showed widespread increases in the availability of cerebral binding sites for the microglial marker, despite normal weight gain compared to the control diet group. Subsequent immunofluorescence staining of the brains confirmed the PET findings, showing a widespread 20% increase in the abundance of IBA-1-positive microglia with characteristic ‘semi-activated’ morphology in the binge sucrose rats, which had 23% lower density of microglial endpoints and 25% lower mean process length compared to microglia in the control rats with ordinary feeding. GFAP immunofluorescence showed no difference in astroglial coverage in the sucrose rats, except for a slight reduction in hypothalamus. The binge sucrose diet-induced neuroinflammation was associated with a significant elevation of white blood cell counts. Taking these results together, we find that long-term intake of sucrose in a binge paradigm, similar in sucrose content to the contemporary Western diet, triggered a low-grade systemic and central inflammation in non-obese rats. The molecular mechanism of this phenomenon remains to be established.https://doi.org/10.1038/s41598-021-90817-z
collection DOAJ
language English
format Article
sources DOAJ
author Omkar L. Patkar
Abdalla Z. Mohamed
Ashwin Narayanan
Karine Mardon
Gary Cowin
Rajiv Bhalla
Damion H. R. Stimson
Michael Kassiou
Kate Beecher
Arnauld Belmer
Ignatius Alvarez Cooper
Michael Morgan
David A. Hume
Katharine M. Irvine
Selena E. Bartlett
Fatima Nasrallah
Paul Cumming
spellingShingle Omkar L. Patkar
Abdalla Z. Mohamed
Ashwin Narayanan
Karine Mardon
Gary Cowin
Rajiv Bhalla
Damion H. R. Stimson
Michael Kassiou
Kate Beecher
Arnauld Belmer
Ignatius Alvarez Cooper
Michael Morgan
David A. Hume
Katharine M. Irvine
Selena E. Bartlett
Fatima Nasrallah
Paul Cumming
A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
Scientific Reports
author_facet Omkar L. Patkar
Abdalla Z. Mohamed
Ashwin Narayanan
Karine Mardon
Gary Cowin
Rajiv Bhalla
Damion H. R. Stimson
Michael Kassiou
Kate Beecher
Arnauld Belmer
Ignatius Alvarez Cooper
Michael Morgan
David A. Hume
Katharine M. Irvine
Selena E. Bartlett
Fatima Nasrallah
Paul Cumming
author_sort Omkar L. Patkar
title A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
title_short A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
title_full A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
title_fullStr A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
title_full_unstemmed A binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
title_sort binge high sucrose diet provokes systemic and cerebral inflammation in rats without inducing obesity
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-05-01
description Abstract While the dire cardiometabolic consequences of the hypercaloric modern ‘Western’ diet are well known, there is not much information on the health impact of a high sucrose diet not inducing weight gain. Here, we tested the hypothesis that rats reared with intermittent binge access to sucrose in addition to normal chow would develop an inflammatory response in brain. To test this hypothesis, we undertook serial PET/MRI scans with the TSPO ligand [18F]DPA714 in a group of (n=9) rats at baseline and again after voluntarily consuming 5% sucrose solution three days a week for three months. Compared to a control group fed with normal chow (n=9), the sucrose rats indeed showed widespread increases in the availability of cerebral binding sites for the microglial marker, despite normal weight gain compared to the control diet group. Subsequent immunofluorescence staining of the brains confirmed the PET findings, showing a widespread 20% increase in the abundance of IBA-1-positive microglia with characteristic ‘semi-activated’ morphology in the binge sucrose rats, which had 23% lower density of microglial endpoints and 25% lower mean process length compared to microglia in the control rats with ordinary feeding. GFAP immunofluorescence showed no difference in astroglial coverage in the sucrose rats, except for a slight reduction in hypothalamus. The binge sucrose diet-induced neuroinflammation was associated with a significant elevation of white blood cell counts. Taking these results together, we find that long-term intake of sucrose in a binge paradigm, similar in sucrose content to the contemporary Western diet, triggered a low-grade systemic and central inflammation in non-obese rats. The molecular mechanism of this phenomenon remains to be established.
url https://doi.org/10.1038/s41598-021-90817-z
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