Hygiene Hampers Competitive Release of Resistant Bacteria in the Commensal Microbiota

Abstract

Good hygiene, in both health care and the community, is central to containing the rise of antibiotic resistance, as well as to infection control more generally. But despite the well-known importance, the ecological mechanisms by which hygiene affects resistance evolution remain obscure. Using metacommunity ecology theory, we here propose that hygiene attenuates the effect of antibiotic selection pressure. Specifically, we predict that hygiene limits the scope for antibiotics to induce competitive release of resistant bacteria within treated hosts, and that this is due to a modulating effect of hygiene on the distribution of resistant and sensitive strains in the host population. We show this in a mathematical model of bacterial metacommunity dynamics, and test the results against data on antibiotic resistance, antibiotic treatment, and the use of alcohol-based hand rub in long-term care facilities. Our results underscore the importance of hygiene, and point to a concrete way to weaken the link between antibiotic use and increasing resistance.

Antibiotics Drive Expansion of Rare Pathogens in a Chronic Infection Microbiome Model

“…Using absolute abundances ( Fig. S4 ), we can now test whether pathogens undergo competitive release (expansion, following removal of competitors [ 75 – 77 ]) in response to antibiotic exposure, by assessing whether the final pathogen density is greater in the presence of antibiotic than in its absence ( Fig. 5 ).…”

Defining the Benefits of Antibiotic Resistance in Commensals and the Scope for Resistance Optimization

“…The reasons are that commensals can horizontally transfer their resistance genes to pathogens ( 9 – 11 ), and in addition, they may themselves cause opportunistic infections ( 12 ). Second, commensals are thought to protect the host from pathogens ( 13 , 14 ), providing colonization resistance ( 15 – 17 ), competitive suppression ( 18 ), and even suppression of pathogen evolution ( 19 – 21 ), but antibiotic treatment disrupts these ecological functions of commensals ( 22 – 24 )—unless they are sufficiently resistant. Hence the tension.…”

Antibiotics drive expansion of rare pathogens in a chronic infection microbiome model

“…Using absolute abundances, we can now test whether pathogens undergo competitive release (expansion, following removal of competitors [77][78][79] ) in response to antibiotic exposure, by assessing whether the final pathogen density is greater in the presence of antibiotic compared to its absence (Figure 4). Comparing mean densities (across replicates), we find evidence for significant competitive release of S. aureus when exposed to tobramycin plus ciprofloxacin (on average a 36-fold increase compared to no-antibiotic control).…”

“…Using absolute abundances, we can now test whether pathogens undergo competitive release (expansion, following removal of competitors [71][72][73] ) in response to antibiotic exposure, by assessing whether the final pathogen density is greater in the presence of antibiotic compared to its absence (Figure 4).…”