An Extra Breath of Fresh Air: Hyperbaric Oxygenation as a Stroke Therapeutic
Abstract
:1. Introduction
2. HBOT in Ischemic Stroke: Potential Benefits and Limitations
2.1. Preclinical Functional Outcomes of Post-stroke HBOT
2.2. Clinical Results of HBOT in Stroke
3. Unpacking Mechanisms of Action of HBOT in Stroke
3.1. Physiological and Metabolic Effects
3.2. Antioxidant Effects
3.3. Anti-Inflammatory Effects
3.4. Additional Neuroprotective Mechanisms
4. Implications of HBOT in Other Neurological and Non-Neurological Conditions
4.1. HBOT in Acute and Chronic TBI
4.2. HBOT in Spinal Cord Injury
4.3. HBOT in Other Pathological Contexts
5. Pre-Clinical Findings with HBOT Preconditioning for Stroke
5.1. Preparation for Oxidative Stress
5.2. Reduction of Apoptosis, Activation of Autophagy, and Promotion of Cell Survival
5.3. Immunosuppression and Immunopreparation
5.4. Preservation of Blood-Brain Barrier, Edema Minimization, and Angiogenesis
5.5. Considerations for HBOT Preconditioning Protocols
6. HBOT-Primed Stem Cells as a Promising Therapy
6.1. HBOT Effects on Endogenous Stem Cells
6.2. HBOT and Exogenous Stem Cells
6.3. Effects of HBOT In Vitro: Potential for Stem Cell Priming
6.4. Recent Literature on HBOT and Stroke
6.4.1. Preconditioning
6.4.2. Post-Stroke Treatment
6.4.3. Diseases Resembling Stroke Pathology and HBOT
6.4.4. Optimizing Treatment
7. Future Directions and Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Study | Discovery |
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Jadhav et al., 2009 | In surgical brain injury (SBI) mice, HBOT preconditioning ameliorated neurological function and cerebral edema; these neuroprotective effects seemed to be regulated by COX-2 mechanisms, as HBOT attenuated SBI-induced elevation of hypoxia-inducible factor-1alpha and COX-2 activity [170]. |
Mu et al., 2013 | In permanent MCAO animal models, daily HBOT conditioning at 48 h post-surgery diminished infarct volume and improved neurological function, which correlated with elevated CREB protein expression in the hippocampus and peri-infarct area, boosting cell multiplication. Regarding acute pMCAo models, HBOT increased cerebral PP1-γ expression, alleviating CREB phosphorylation and ubiquitination spurred by ischemia. Moreover, HBOT’s regenerative effects against ischemic stroke can be associated with CREB and PP1-γ mechanisms [37]. |
Lu et al., 2014 | In transient MCAO rat models, HBOT spurred an increase in ERK1/2 signaling due to higher levels of ROS, leading to the attenuation of autophagy. When U0126, an inhibitor of the ERK1/2 pathway, was applied, infarct size and autophagy were ameliorated [171]. |
Xue et al., 2016 | MCAO rats subjected to HBOT preconditioning exhibited diminished infarct size, improved neurological behavior, and upregulated Sirt1, Nrf2, HO-1, and SOD1 expression, as well as reduction of MDA. Blocking of Sirt1 or Nrf2 abolished HBOT-induced protective effects, as Nrf2, HO-1, and SOD1 were repressed. Moreover, the protective actions of Sirt1, spurred by HBOT, may consist of the Nrf2/antioxidant defense mechanism [172]. |
Guo et al., 2016 | Following successive HBOT pre-treatment over five days, rats underwent hyperglycemic MCAO. Preconditioning with HBOT significantly ameliorated hemorrhagic transformation induced by the Nod-like receptor protein 3 signaling and reduced infarct size, altogether rehabilitating neurological performance. HBOT’s neuroprotective effects could be linked to the ROS/thioredoxin-interacting protein/Nod-like receptor protein 3 mechanism [126]. |
Yang et al., 2017 | HBOT ameliorated neurological impairment in TBI rats via upregulation of VEGF, VEGFR2, Raf-1, MEK1/2, and ERK1/2, stimulating proliferation of neural stem cells (NSC) and homing of these cells to the lesion site. The examination of HBOT’s protective effects in vitro showed similar results, as HBO drastically amplified NSC proliferation and VEGF/ERK signaling [123]. |
Hu et al., 2017 | In hyperglycemia MCAO rats, exposure to two atmospheres of HBO for an hour immediately after dextrose administration ameliorated depleted ATP and nitcotinamide adenine dinucleotide levels, which in turn elevated silent mating type information regulation 2 homolog 1, alleviating cerebral infarct and neurological dysfunction, along with repressing hemorrhagic transformation [14]. |
He et al., 2019 | Mice models of acute TBI demonstrated escalated levels of apoptotic neurons and caspase-3 activity, along with attenuation of signaling pathways that regulate apoptosis in neurons (e.g., pAkt/Akt, pGSK3β/GSK3β, and β-catenin). By eliminating the TBI-induced alterations in these pathways, HBOT suppressed neuronal apoptosis [173]. |
Ying et al., 2019 | BDNF/TrkB signaling has been shown to influence rehabilitation after SCI. In vivo, SCI rat models were exposed to HBOT, and both dendritic/synaptic deterioration and apoptosis were ameliorated, which could be linked to higher levels of BDNF and TrkB activity. When ANA-12, an inhibitor of the BDNF/TrkB pathway, was administered, HBOT’s neuroprotective effects were reversed, indicating that HBOT’s therapeutic benefits are mediated by BDNF/TrkB signaling [174]. |
Zhou et al., 2019 | Following HBOT, Sprague-Dawley rats with spinal cord injury (SCI) displayed ameliorated motor function and attenuated secondary injuries, such as inflammation and glial scar production. By blocking AKT and NF-kB signaling, HBOT repressed molecules associated with inflammation (iNOS and COX-2) and glial scar generation (GFAP and NG2) [175]. |
Study | Discovery |
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Yang et al., 2008 | Rats were subject to unilateral carotid artery ligation and then 2 h of hypoxia. HBO2 was then administered following the hypoxic-ischemic event. The HBOT was found to upregulate neural stem cell proliferation in neurogenic environments within the adult brain [143]. |
Li et al., 2008 | A murine model subjected rats to common carotid artery ligation and hypoxia for 90 min. HBOT was administered 24 h prior to the hypoxic-ischemic injury. Results revealed that rats preconditioned with HBOT had an increased survival rate, and the infarct ratio was decreased. This indicates that HBOT can provide brain protection via the inhibition of neuronal apoptosis pathways [45]. |
Li et al., 2009 | HBOT preconditioned rats where investigated to determine if apoptotic inhibition through a mitochondrial pathway was correlated with neuroprotection in the ischemic injury in the rat brain. Preconditioning was conducted four times, followed by brain evaluation. Results indicated that HBO-PC significantly reduced brain edema and decreased infarction volume and improved neurological recovery [117]. |
Rink et al., 2010 | Transient MCAO rodents outline the therapeutic potential of normobaric and hyperbaric oxygen treatments during ischemia and after ischemia. HBOT-treated rodents revealed inhibited leukocyte accumulation in the ischemic area due to a reduction in levels of inflammatory chemokines [50]. |
Cechin et al., 2014 | This study allowed pancreatic progenitor cells to mature in a perfluorocarbon-based culture device that could adjust the levels of pO2. Enhanced O2 exposure in vitro led to maturation and differentiation of human embryonic stem cell-derived pancreatic progenitor cells [176]. |
Hadanny et al., 2015 | Patients with cardiac arrest-induced chronic cognitive impairments where treated with sessions of HBOT and analyzed. After administering HBOT five days per week to chronic stroke patients, patients had significant improvements in memory and attention testing [22]. |
Dai et al., 2015 | A rabbit model seeded human adipose-derived stem cells on a gelatin/polycaprolactone scaffold to determine the functional and histochemical improvement of tissue-engineered cartilage after HBOT. The human adipose-derived stem cells were found to have improved extracellular matrix-secreting abilities after transplantation into a rabbit cartilage defect model when primed with HBOT [177]. |
Yang et al., 2017 | This study investigated the mechanism of HBOT that promote NSC proliferation and recovery following TBI. The study used 24 rats split into a sham group, a TBI group, and an HBO treated TBI group to determine the neurological differences. Neurological function was evaluated and monitored throughout the week. HBOT was found to promote neural stem cell migration to areas of injury within the brain in rat models of TBI that were preconditioned with HBO [123]. |
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Cozene, B.; Sadanandan, N.; Gonzales-Portillo, B.; Saft, M.; Cho, J.; Park, Y.J.; Borlongan, C.V. An Extra Breath of Fresh Air: Hyperbaric Oxygenation as a Stroke Therapeutic. Biomolecules 2020, 10, 1279. https://doi.org/10.3390/biom10091279
Cozene B, Sadanandan N, Gonzales-Portillo B, Saft M, Cho J, Park YJ, Borlongan CV. An Extra Breath of Fresh Air: Hyperbaric Oxygenation as a Stroke Therapeutic. Biomolecules. 2020; 10(9):1279. https://doi.org/10.3390/biom10091279
Chicago/Turabian StyleCozene, Blaise, Nadia Sadanandan, Bella Gonzales-Portillo, Madeline Saft, Justin Cho, You Jeong Park, and Cesar V. Borlongan. 2020. "An Extra Breath of Fresh Air: Hyperbaric Oxygenation as a Stroke Therapeutic" Biomolecules 10, no. 9: 1279. https://doi.org/10.3390/biom10091279