Electrical vagus nerve stimulation attenuates systemic inflammation and improves survival in a rat heatstroke model

PLoS One. 2013;8(2):e56728. doi: 10.1371/journal.pone.0056728. Epub 2013 Feb 12.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD11b Antigen / metabolism
  • Disease Models, Animal
  • Electric Stimulation Therapy / methods*
  • Endothelial Cells / metabolism
  • Gene Expression Regulation
  • Heat Stroke / complications*
  • Heat Stroke / metabolism
  • Heat Stroke / pathology
  • Heat Stroke / therapy*
  • Heat-Shock Response
  • Inflammation / complications
  • Lung / pathology
  • Male
  • Rats
  • Rats, Wistar
  • Receptors, Nicotinic / metabolism
  • Spleen / pathology
  • Survival Analysis
  • Vagus Nerve*
  • alpha7 Nicotinic Acetylcholine Receptor

Substances

  • CD11b Antigen
  • Chrna7 protein, rat
  • Receptors, Nicotinic
  • alpha7 Nicotinic Acetylcholine Receptor

Grants and funding

This study was supported by a Grant-in-aid for scientific research from the Ministry of Education, Culture, Sports, Science, and Technology in Japan (No. 24791938). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.