Bacterial biofilms predominate in both acute and chronic human lung infections

Abstract

BackgroundA basic paradigm of human infection is that acute bacterial disease is caused by fast growing planktonic bacteria while chronic infections are caused by slow-growing, aggregated bacteria, a phenomenon known as a biofilm. For lung infections, this paradigm has been thought to be supported by observations of how bacteria proliferate in well-established growth media in the laboratory—the gold standard of microbiology.ObjectiveTo investigate the bacterial architecture in sputum from patients with acute and chronic lung infections.MethodsAdvanced imaging technology was used for quantification and direct comparison of infection types on fresh sputum samples, thereby directly testing the acute versus chronic paradigm.ResultsIn this study, we compared the bacterial lifestyle (planktonic or biofilm), growth rate and inflammatory response of bacteria in freshly collected sputum (n=43) from patient groups presenting with acute or chronic lung infections. We found that both acute and chronic lung infections are dominated by biofilms (aggregates of bacteria within an extracellular matrix), although planktonic cells were observed in both sample types. Bacteria grew faster in sputum from acute infections, but these fast-growing bacteria were enriched in biofilms similar to the architecture thought to be reserved for chronic infections. Cellular inflammation in the lungs was also similar across patient groups, but systemic inflammatory markers were only elevated in acute infections.ConclusionsOur findings indicate that the current paradigm of equating planktonic with acute and biofilm with chronic infection needs to be revisited as the difference lies primarily in metabolic rates, not bacterial architecture.

Pseudomonas aeruginosacontracts mucus to form biofilms in tissue-engineered human airways

“…Active mucus contraction by P. aeruginosa speeds up biofilm formation compared to axenic conditions. Although the classical view of airway infections associates biofilms with chronic infections and planktonic cells with acute infections, recent work has demonstrated the coexistence of these bacterial lifestyles in sputum samples from both acutely and chronically infected patients 40 . Our observations of rapid biofilm formation in both healthy and CF AirGels is consistent with these clinical observations.…”

Prevalence of biofilms in acute infections challenges a longstanding paradigm

“…While the predominance of the biofilm lifestyle in chronic infections was confirmed, the prevalence of the biofilm lifestyle in acute infections has recently been challenged in a comparison between chronic and acute lung infections [ 11 ] ( Fig. 1 ).…”

“…These observations suggest that we need a new bacterial infection paradigm. Since the bacterial growth rate was found to be different in chronic and acute infections [ 11 ], we propose the new paradigm to emphasize on characterization of the infections according to the bacterial metabolism rather than bacterial aggregation. In chronic lung infections the growth of biofilm forming bacteria is linked to the activity of the inflammatory cells [ 8 , 9 ].…”

“…Scale bar is 10 μm. [ 11 ]. (D) Representative scanning electronmicrographs of GAS biofilm and non biofilm single-cocci are as in patient biopsies.…”

“…However, the role of EPS changes temporally over the course of an infection as EPS loses its impact on virulence which is highest in acute infections [ 23 ]. However, this has not been demonstrated in acute and chronic pneumonia where EPS was detected in both infection types [ 11 ].…”