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Hyperbaric Oxygen Treatment Produces an Antinociceptive Response Phase and Inhibits Astrocyte Activation and Inflammatory Response in a Rat Model of Neuropathic Pain

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Abstract

Hyperbaric oxygen (HBO) treatment has been proven to be a promising candidate for protection of the nervous system after acute injury in animal models of neuropathic pain. The purposes of this study were to examine the antinociceptive response phase induced by HBO treatment in a model of neuropathic pain and to determine the dependence of the treatment's mechanism of alleviating neuropathic pain on the inhibition of spinal astrocyte activation. Neuropathic pain was induced in rats by chronic constriction injury of the sciatic nerve. Mechanical threshold and thermal latency were tested preoperatively and for 1 week postoperatively, four times daily at fixed time points. Methane dicarboxylic aldehyde (MDA) and superoxide dismutase (SOD) parameters were used as indices of oxidative stress response and tested before and after the treatment. The inflammatory cytokines interleukin (IL)-1β and IL-10 were assayed in the sciatic nerve were with enzyme-linked immunoassay. Glial fibrillary acidic protein activation in the spinal cord was evaluated immunohistochemically. The rats exhibited temporary allodynia immediately after HBO treatment completion. This transient allodynia was closely associated with changes in MDA and SOD levels. A single HBO treatment caused a short-acting antinociceptive response phase. Repetitive HBO treatment led to a long-acting antinociceptive response phase and inhibited astrocyte activation. These results indicated that HBO treatment played a dual role in the aggravation and alleviation of neuropathic pain, though the aggravated pain effect (transient allodynia) was far less pronounced than the antinociceptive phase. Astrocyte inhibition and anti-inflammation may contribute to the antinociceptive effect of HBO treatment after nerve injury.

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Abbreviations

HBO:

Hyperbaric oxygen

TNF:

Tumor necrosis factor

CCI:

Chronic constriction injury

ATA:

Atmospheres absolute pressure

MWT:

Mechanical withdrawal threshold

TWL:

Thermal withdrawal latency

AB:

Avidin-biotin

GFAP:

Glial fibrillary acidic protein

ROS:

Oxygen species

CREB:

cAMP response element-binding protein

MDA:

Methane dicarboxylic aldehyde

SOD:

Superoxide dismutase

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Acknowledgments

This work was supported by the Science and Technology Plan Project and B. Braun Anesthesia Scientific Research Fund (grant no. F10-205-1-41 and BBF 2012-012). We thank Dr. Cui Jian-Jun for supporting this study.

Conflict of Interest

There are no ethical/legal conflicts involved in the article.

Author information

Authors and Affiliations

  1. Department of Anesthesiology, China Medical University, Shengjing Hospital, 110004, Shenyang, China

    Bai-Song Zhao, Ling-Xin Meng & Yan-Yan Cao

  2. Department of Pain, China Medical University, Shengjing Hospital, 110004, Shenyang, China

    Yuan-Yuan Ding

Authors
  1. Bai-Song Zhao
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  2. Ling-Xin Meng
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  3. Yuan-Yuan Ding
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  4. Yan-Yan Cao
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Correspondence to Bai-Song Zhao.

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A short note

HBO treatment may be an important intervention for preventing neuronal damage. Recent studies have reported that HBO treatment can increase neuroplasticity leading to repair of chronically impaired brain functions and improved quality of life in patients who have experienced traumatic brain injury with prolonged post-concussion syndrome even in a late chronic stage. Furthermore, HBO can lead to significant neurological improvements in stroke patients, including chronic late-stage stroke patients. The observed clinical improvements suggest that HBO therapy after brain damage favors the repair of nervous tissue and function. The results presented in this paper may pave the way for future experimental studies, including research addressing HBO therapy efficacy in peripheral versus central nervous system damage.

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Zhao, BS., Meng, LX., Ding, YY. et al. Hyperbaric Oxygen Treatment Produces an Antinociceptive Response Phase and Inhibits Astrocyte Activation and Inflammatory Response in a Rat Model of Neuropathic Pain. J Mol Neurosci 53, 251–261 (2014). https://doi.org/10.1007/s12031-013-0213-3

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  • DOI: https://doi.org/10.1007/s12031-013-0213-3

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