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Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model

This study was performed to gain insights into novel therapeutic approaches for the treatment of heatstroke. The central nervous system regulates peripheral immune responses via the vagus nerve, the primary neural component of the cholinergic anti-inflammatory pathway. Electrical vagus nerve stimula...

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Autores principales: Yamakawa, Kazuma, Matsumoto, Naoya, Imamura, Yukio, Muroya, Takashi, Yamada, Tomoki, Nakagawa, Junichiro, Shimazaki, Junya, Ogura, Hiroshi, Kuwagata, Yasuyuki, Shimazu, Takeshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3570456/
https://www.ncbi.nlm.nih.gov/pubmed/23424673
http://dx.doi.org/10.1371/journal.pone.0056728
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author Yamakawa, Kazuma
Matsumoto, Naoya
Imamura, Yukio
Muroya, Takashi
Yamada, Tomoki
Nakagawa, Junichiro
Shimazaki, Junya
Ogura, Hiroshi
Kuwagata, Yasuyuki
Shimazu, Takeshi
author_facet Yamakawa, Kazuma
Matsumoto, Naoya
Imamura, Yukio
Muroya, Takashi
Yamada, Tomoki
Nakagawa, Junichiro
Shimazaki, Junya
Ogura, Hiroshi
Kuwagata, Yasuyuki
Shimazu, Takeshi
author_sort Yamakawa, Kazuma
collection PubMed
description This study was performed to gain insights into novel therapeutic approaches for the treatment of heatstroke. The central nervous system regulates peripheral immune responses via the vagus nerve, the primary neural component of the cholinergic anti-inflammatory pathway. Electrical vagus nerve stimulation (VNS) reportedly suppresses pro-inflammatory cytokine release in several models of inflammatory disease. Here, we evaluated whether electrical VNS attenuates severe heatstroke, which induces a systemic inflammatory response. Anesthetized rats were subjected to heat stress (41.5°C for 30 minutes) with/without electrical VNS. In the VNS-treated group, the cervical vagus nerve was stimulated with constant voltage (10 V, 2 ms, 5 Hz) for 20 minutes immediately after completion of heat stress. Sham-operated animals underwent the same procedure without stimulation under a normothermic condition. Seven-day mortality improved significantly in the VNS-treated group versus control group. Electrical VNS significantly suppressed induction of pro-inflammatory cytokines such as tumor necrosis factor-α and interleukin-6 in the serum 6 hours after heat stress. Simultaneously, the increase of soluble thrombomodulin and E-selectin following heat stress was also suppressed by VNS treatment, suggesting its protective effect on endothelium. Immunohistochemical analysis using tissue preparations obtained 6 hours after heat stress revealed that VNS treatment attenuated infiltration of inflammatory (CD11b-positive) cells in lung and spleen. Interestingly, most cells with increased CD11b positivity in response to heat stress did not express α7 nicotinic acetylcholine receptor in the spleen. These data indicate that electrical VNS modulated cholinergic anti-inflammatory pathway abnormalities induced by heat stress, and this protective effect was associated with improved mortality. These findings may provide a novel therapeutic strategy to combat severe heatstroke in the critical care setting.
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spelling pubmed-35704562013-02-19 Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model Yamakawa, Kazuma Matsumoto, Naoya Imamura, Yukio Muroya, Takashi Yamada, Tomoki Nakagawa, Junichiro Shimazaki, Junya Ogura, Hiroshi Kuwagata, Yasuyuki Shimazu, Takeshi PLoS One Research Article This study was performed to gain insights into novel therapeutic approaches for the treatment of heatstroke. The central nervous system regulates peripheral immune responses via the vagus nerve, the primary neural component of the cholinergic anti-inflammatory pathway. Electrical vagus nerve stimulation (VNS) reportedly suppresses pro-inflammatory cytokine release in several models of inflammatory disease. Here, we evaluated whether electrical VNS attenuates severe heatstroke, which induces a systemic inflammatory response. Anesthetized rats were subjected to heat stress (41.5°C for 30 minutes) with/without electrical VNS. In the VNS-treated group, the cervical vagus nerve was stimulated with constant voltage (10 V, 2 ms, 5 Hz) for 20 minutes immediately after completion of heat stress. Sham-operated animals underwent the same procedure without stimulation under a normothermic condition. Seven-day mortality improved significantly in the VNS-treated group versus control group. Electrical VNS significantly suppressed induction of pro-inflammatory cytokines such as tumor necrosis factor-α and interleukin-6 in the serum 6 hours after heat stress. Simultaneously, the increase of soluble thrombomodulin and E-selectin following heat stress was also suppressed by VNS treatment, suggesting its protective effect on endothelium. Immunohistochemical analysis using tissue preparations obtained 6 hours after heat stress revealed that VNS treatment attenuated infiltration of inflammatory (CD11b-positive) cells in lung and spleen. Interestingly, most cells with increased CD11b positivity in response to heat stress did not express α7 nicotinic acetylcholine receptor in the spleen. These data indicate that electrical VNS modulated cholinergic anti-inflammatory pathway abnormalities induced by heat stress, and this protective effect was associated with improved mortality. These findings may provide a novel therapeutic strategy to combat severe heatstroke in the critical care setting. Public Library of Science 2013-02-12 /pmc/articles/PMC3570456/ /pubmed/23424673 http://dx.doi.org/10.1371/journal.pone.0056728 Text en © 2013 Yamakawa et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Yamakawa, Kazuma
Matsumoto, Naoya
Imamura, Yukio
Muroya, Takashi
Yamada, Tomoki
Nakagawa, Junichiro
Shimazaki, Junya
Ogura, Hiroshi
Kuwagata, Yasuyuki
Shimazu, Takeshi
Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title_full Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title_fullStr Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title_full_unstemmed Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title_short Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model
title_sort electrical vagus nerve stimulation attenuates systemic inflammation and improves survival in a rat heatstroke model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3570456/
https://www.ncbi.nlm.nih.gov/pubmed/23424673
http://dx.doi.org/10.1371/journal.pone.0056728
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