Bacterial biofilms predominate in both acute and chronic human lung infections

Author:

Kolpen MetteORCID,Kragh Kasper Nørskov,Enciso Juan Barraza,Faurholt-Jepsen Daniel,Lindegaard Birgitte,Egelund Gertrud Baunbæk,Jensen Andreas Vestergaard,Ravn Pernille,Mathiesen Inger Hee Mabuza,Gheorge Alexandra Gabriella,Hertz Frederik Boëtius,Qvist Tavs,Whiteley Marvin,Jensen Peter Østrup,Bjarnsholt ThomasORCID

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.

Funder

Lundbeck Foundation

Olga Brydes Foundation

Cystic Fibrosis Foundation Therapeutics

Foundation for the National Institutes of Health

Novo Nordisk Foundation Tandem Program

Technology and Production Sciences

Human Frontiers Science Program

Nordsjællands University Hospital

Publisher

BMJ

Subject

Pulmonary and Respiratory Medicine

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