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Pulmonary and Non-Pulmonary Sepsis Differentially Modulate Lung Immunity Towards Secondary Bacterial Pneumonia: A Critical Role for Alveolar Macrophages.
Clinical observations suggest that the source of primary infection accounts for a major determinant of further nosocomial pneumonia in critically ill sepsis patients. We herein addressed the impact of primary non-pulmonary or pulmonary septic insults on lung immunity using relevant double-hit animal models. C57BL/6J mice were first subjected to either polymicrobial peritonitis induced by caecal ligation and puncture (CLP) or bacterial pneumonia induced by intratracheal challenge with Escherichia coli. Seven days after, post-septic mice received intratracheal challenge with Pseudomonas aeruginosa. When compared to controls, post-CLP mice became highly susceptible to P. aeruginosa pneumonia as demonstrated by defective lung bacterial clearance and increased mortality rate. In contrast, all post-pneumonia mice survived the P. aeruginosa challenge and even exhibited improved bacterial clearance. Non-pulmonary and pulmonary sepsis differentially modulated the amounts and some important immune functions of alveolar macrophages. Additionally, we observed a Toll-like receptor 2 (TLR2)-dependent increase in regulatory T cells (Tregs) in lungs from post-CLP mice. Antibody-mediated Tregs depletion restored the numbers and functions of alveolar macrophages in post-CLP mice. Furthermore, post-CLP TLR2-deficient mice were found resistant to secondary P. aeruginosa pneumonia. In conclusion, polymicrobial peritonitis and bacterial pneumonia conferred susceptibility or resistance to secondary Gram-negative pulmonary infection, respectively. Immune patterns in post-CLP lungs argue for a TLR2-dependent crosstalk between T-regs and alveolar macrophages, as an important regulatory mechanism in post-septic lung defense.
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