Metapopulation ecology links antibiotic resistance, consumption, and patient transfers in a network of hospital wards

Abstract

Antimicrobial resistance (AMR) is a global threat. A better understanding of how antibiotic use and between-ward patient transfers (or connectivity) impact population-level AMR in hospital networks can help optimize antibiotic stewardship and infection control strategies. Here, we used a metapopulation framework to explain variations in the incidence of infections caused by 7 major bacterial species and their drug-resistant variants in a network of 357 hospital wards. We found that ward-level antibiotic consumption volume had a stronger influence on the incidence of the more resistant pathogens, while connectivity had the most influence on hospital-endemic species and carbapenem-resistant pathogens. Piperacillin-tazobactam consumption was the strongest predictor of the cumulative incidence of infections resistant to empirical sepsis therapy. Our data provide evidence that both antibiotic use and connectivity measurably influence hospital AMR. Finally, we provide a ranking of key antibiotics by their estimated population-level impact on AMR that might help inform antimicrobial stewardship strategies.

Exceptions to the rule: Why does resistance evolution not undermine antibiotic therapy in all bacterial infections?

“…While we were able to identify factors that associate with elevated or reduced levels of resistance at such large scales, we note that over shorter timescales and more localized spatial scales key factors may differ. For example, we did not find an effect of total drug use on resistance, but drug use is known to drive resistance increases at finer scales such as within individual hospitals or countries 30,52,53 . We also note that being an observational study, the associations identified here are not necessarily causative.…”

“…In fact, our results demonstrate that among the various factors implicated in resistance evolution, being nosocomial is one of the most statistically robust predictors (Table 2). The high prevalence of antibiotic resistance among nosocomial pathogens is largely attributed to the interplay of high antibiotic usage, which may impose selection for resistance, and imperfect infection control practices, which may promote transmission of resistant pathogens in hospitals [29][30][31] . These results highlight the importance of developing protocols to further minimize pathogen transmission within hospitals, for example, by improving sterilization and hygiene practices.…”

Microbiome-pathogen interactions drive epidemiological dynamics of antibiotic resistance: A modeling study applied to nosocomial pathogen control

“…Nonetheless, our goal was to study how ecological mechanisms impact average epidemiological outcomes in the context of different model assumptions and parameter uncertainty, and in this context, ODE modeling was the more appropriate tool, particularly for widely endemic ARB like C. difficile , MRSA and ESBL-EC. Still, further insights could certainly be gained by accounting for additional complexity and stochastic heterogeneity in future work, from within-host spatial organization ( Estrela et al, 2015 ), to patient and staff contact behavior ( Duval et al, 2019 ), to inter-institutional or inter-ward meta-population dynamics ( Shapiro et al, 2020 ). These distinctions may be particularly important for rare or non-endemic ARB (e.g.…”

“…(Niewiadomska et al, 2019) Here, microbiome competition was found to have a large impact on incidence but comparatively little impact on resistance ratesboth for the theoretical pathogen evaluated in Part 1 (Figures 3, 4) and for the four ARB (Estrela et al, 2015) to patient and staff contact behaviour, (Duval et al, 2019) to inter-institutional or inter-ward meta-population dynamics. (Shapiro et al, 2020) These distinctions may be particularly important for rare or nonendemic ARB (e.g. CP-KP in some regions).…”

Modelling how antimicrobial resistance spreads between wards

“…Now, in eLife, Jean-Philippe Rasigade and co-workers from Université de Lyon and the Hospices Civils de Lyon – including Julie Teresa Shapiro as first author – report how seven species of bacteria, and their resistant strains, spread across 357 wards of a major hospital organisation in Lyon ( Shapiro et al, 2020 ). To do this, the team adapted a model that is often used in ecology to study populations of animal species that live in, and migrate between, different locations.…”