A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats

Persistent post-surgical pain (PPSP) occurs in a proportion of patients following surgical interventions. Research suggests that specific microbiome components are important for brain development and function, with recent studies demonstrating that chronic pain results in changes to the microbiome....

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Main Authors: Sabrina Salberg, Matthew Macowan, Angela Doshen, Glenn R. Yamakawa, Marissa Sgro, Benjamin Marsland, Luke A. Henderson, Richelle Mychasiuk
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S105381192500059X
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author Sabrina Salberg
Matthew Macowan
Angela Doshen
Glenn R. Yamakawa
Marissa Sgro
Benjamin Marsland
Luke A. Henderson
Richelle Mychasiuk
author_facet Sabrina Salberg
Matthew Macowan
Angela Doshen
Glenn R. Yamakawa
Marissa Sgro
Benjamin Marsland
Luke A. Henderson
Richelle Mychasiuk
author_sort Sabrina Salberg
collection DOAJ
description Persistent post-surgical pain (PPSP) occurs in a proportion of patients following surgical interventions. Research suggests that specific microbiome components are important for brain development and function, with recent studies demonstrating that chronic pain results in changes to the microbiome. Consumption of a high fat, high sugar (HFHS) diet can drastically alter composition of the microbiome and is a modifiable risk factor for many neuroinflammatory conditions. Therefore, we investigated how daily consumption of a HFHS diet modified the development of PPSP, brain structure and function, and the microbiome. In addition, we identified significant correlations between the microbiome and brain in animals with PPSP. Male and female rats were maintained on a control or HFHS diet. Animals were further allocated to a sham or surgery on postnatal day (p) p35. The von Frey task measured mechanical nociceptive sensitivity at a chronic timepoint (p65–67). Between p68–72 rats underwent in-vivo MRI to examine brain volume and diffusivity. At p73 fecal samples were used for downstream 16 s rRNA sequencing. Spearman correlation analyses were performed between individual microbial abundance and MRI diffusivity to determine if specific bacterial species were associated with PPSP-induced brain changes. We found that consumption of a HFHS diet exacerbated PPSP in adolescents. The HFHS diet reduced overall brain volume and increased white and grey matter density. The HFHS diet interacted with the surgical intervention to modify diffusivity in numerous brain regions which were associated with specific changes to the microbiome. These findings demonstrate that premorbid characteristics can influence the development of PPSP and advance our understanding of the contribution that the microbiome has on function of the brain-microbiota-gut axis.
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spelling doaj-art-bd72386ec49649a6be6f77ac7ec7fbc02025-02-06T05:11:10ZengElsevierNeuroImage1095-95722025-02-01307121057A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent ratsSabrina Salberg0Matthew Macowan1Angela Doshen2Glenn R. Yamakawa3Marissa Sgro4Benjamin Marsland5Luke A. Henderson6Richelle Mychasiuk7Department of Neuroscience, Monash University, Melbourne, VIC, Australia; Gastroenterology, Immunology, Neuroscience (GIN) Discovery Program, AustraliaGastroenterology, Immunology, Neuroscience (GIN) Discovery Program, Australia; Department of Immunology, Monash University, Melbourne, VIC, AustraliaSchool of Medical Sciences (Neuroscience), Brain and Mind Centre, University of Sydney, NSW, AustraliaDepartment of Neuroscience, Monash University, Melbourne, VIC, Australia; Gastroenterology, Immunology, Neuroscience (GIN) Discovery Program, AustraliaDepartment of Neuroscience, Monash University, Melbourne, VIC, Australia; Gastroenterology, Immunology, Neuroscience (GIN) Discovery Program, AustraliaGastroenterology, Immunology, Neuroscience (GIN) Discovery Program, Australia; Department of Immunology, Monash University, Melbourne, VIC, AustraliaSchool of Medical Sciences (Neuroscience), Brain and Mind Centre, University of Sydney, NSW, AustraliaDepartment of Neuroscience, Monash University, Melbourne, VIC, Australia; Gastroenterology, Immunology, Neuroscience (GIN) Discovery Program, Australia; Corresponding author at: Department of Neuroscience, Central Clinical School, Monash University, 6th Floor, 99 Commercial Road, Melbourne VIC, 3004.Persistent post-surgical pain (PPSP) occurs in a proportion of patients following surgical interventions. Research suggests that specific microbiome components are important for brain development and function, with recent studies demonstrating that chronic pain results in changes to the microbiome. Consumption of a high fat, high sugar (HFHS) diet can drastically alter composition of the microbiome and is a modifiable risk factor for many neuroinflammatory conditions. Therefore, we investigated how daily consumption of a HFHS diet modified the development of PPSP, brain structure and function, and the microbiome. In addition, we identified significant correlations between the microbiome and brain in animals with PPSP. Male and female rats were maintained on a control or HFHS diet. Animals were further allocated to a sham or surgery on postnatal day (p) p35. The von Frey task measured mechanical nociceptive sensitivity at a chronic timepoint (p65–67). Between p68–72 rats underwent in-vivo MRI to examine brain volume and diffusivity. At p73 fecal samples were used for downstream 16 s rRNA sequencing. Spearman correlation analyses were performed between individual microbial abundance and MRI diffusivity to determine if specific bacterial species were associated with PPSP-induced brain changes. We found that consumption of a HFHS diet exacerbated PPSP in adolescents. The HFHS diet reduced overall brain volume and increased white and grey matter density. The HFHS diet interacted with the surgical intervention to modify diffusivity in numerous brain regions which were associated with specific changes to the microbiome. These findings demonstrate that premorbid characteristics can influence the development of PPSP and advance our understanding of the contribution that the microbiome has on function of the brain-microbiota-gut axis.http://www.sciencedirect.com/science/article/pii/S105381192500059XMRI16s rRNADiffusivityAkkermansiaBacteroidesNociception
spellingShingle Sabrina Salberg
Matthew Macowan
Angela Doshen
Glenn R. Yamakawa
Marissa Sgro
Benjamin Marsland
Luke A. Henderson
Richelle Mychasiuk
A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
NeuroImage
MRI
16s rRNA
Diffusivity
Akkermansia
Bacteroides
Nociception
title A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
title_full A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
title_fullStr A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
title_full_unstemmed A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
title_short A high fat, high sugar diet exacerbates persistent post-surgical pain and modifies the brain-microbiota-gut axis in adolescent rats
title_sort high fat high sugar diet exacerbates persistent post surgical pain and modifies the brain microbiota gut axis in adolescent rats
topic MRI
16s rRNA
Diffusivity
Akkermansia
Bacteroides
Nociception
url http://www.sciencedirect.com/science/article/pii/S105381192500059X
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