Postnatal Azithromycin Is Neuroprotective and Anti-Inflammatory in a Piglet Model of Hypoxic-Ischemic Encephalopathy

产后阿奇霉素在缺氧缺血性脑病仔猪模型中具有神经保护和抗炎作用

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Abstract

BACKGROUND: There is an urgent need for cytoprotective therapies for hypoxic-ischemic encephalopathy in low- and middle-income countries, where therapeutic hypothermia is not beneficial. Infection and inflammation are important risk factors for hypoxic-ischemic encephalopathy in sub-Saharan Africa, and immunomodulatory therapies might improve outcomes. Azithromycin is neuroprotective in rodent hypoxic-ischemic encephalopathy models but validation in large animal models is needed. Our aim was to assess safety and efficacy of intravenous azithromycin after inflammation-amplified hypoxia-ischemia in newborn piglets. METHODS: Twenty-five piglets underwent inflammation-amplified hypoxia-ischemia by bilateral carotid artery occlusion and reduction in FiO(2) to 6% at 4 hours after the start of Escherichia coli liposaccharide infusion (2 mcg/kg bolus+1 mcg/kg per hour over 12 hours). At 1 hour after inflammation-amplified hypoxia-ischemia, piglets were randomized to receive vehicle (n=12) or azithromycin 20 mg/kg over 1 hour (n=13), repeated at 24 and 48 hours. Piglets underwent neurocritical care for 65 hours, including continuous amplitude-integrated encephalography, magnetic resonance imaging/magnetic resonance spectroscopy at 60 hours, and brain immunohistochemistry. Group differences were evaluated by Bayesian analysis with noninformative priors; the a priori threshold probability of superiority (Pr([)(sup])) was set at 95%. RESULTS: Insult severity did not differ between groups. Plasma azithromycin peak concentration (C(max)) of ≈2 mg/mL and brain tissue concentrations of ≈1.5 mg/kg were achieved. Azithromycin was associated with improved amplitude-integrated encephalography background (Pr([)(sup])=98.6%), an overall increase in neuronal nuclear antigen (NeuN+) cells (Pr([)(sup])=97.8%), increase in Iba1 (ionized calcium-binding adapter molecule 1)+cells (Pr([)(sup])=99.6%) and increase in Iba1 ramification index (resting microglial morphology; Pr([)(sup)(])=99.6%). The treatment benefit on magnetic resonance spectroscopy lactate to N-acetyl aspartate peak area ratio was modest (Pr([)(sup]) of 82.7% and 68.5% in the thalamic and white matter voxels, respectively). CONCLUSIONS: Azithromycin, administered after inflammation-amplified hypoxia-ischemia was safe and associated with increased neuronal survival, microglial immunomodulation, enhanced amplitude-integrated encephalography recovery, and a modest benefit on lactate to N-acetyl aspartate peak area ratio. These safety and efficacy data of azithromycin as a monotherapy hold promise to improve outcomes for hypoxic-ischemic encephalopathy in low- and middle-income countries.

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