Hypoxia arising from concerted oxygen consumption by neutrophils and microorganisms in biofilms

Abstract

Infections associated with microbial biofilms are often found to involve hypoxic or anoxic conditions within the biofilm or its vicinity. To shed light on the phenomenon of local oxygen depletion, mathematical reaction-diffusion models were derived that integrated the two principal oxygen sinks, microbial respiration and neutrophil consumption. Three simple one-dimensional problems were analyzed approximating biofilm near an air interface as in a dermal wound or mucus layer, biofilm on an implanted medical device, or biofilm aggregates dispersed in mucus or tissue. In all three geometries considered, hypoxia at the biofilm–neutrophil interface or within the biofilm was predicted for a subset of plausible parameter values. The finding that oxygen concentration at the biofilm–neutrophil juncture can be diminished to hypoxic levels is biologically relevant because oxygen depletion will reduce neutrophil killing ability. The finding that hypoxia can readily establish in the interior of the biofilm is biologically relevant because this change will alter microbial metabolism and persistence.