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Spatiotemporal Dynamics of Multidrug Resistant Bacteria on Intensive Care Unit Surfaces

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Spatiotemporal Dynamics of Multidrug Resistant Bacteria on Intensive Care Unit Surfaces Washington University School of Medicine Digital Commons@Becker Open Access Publications 2019 Spatiotemporal dynamics of multidrug resistant bacteria on intensive care unit surfaces Alaric W. D'Souza Robert F. Potter Meghan Wallace Angela Shupe Sanket Patel See next page for additional authors Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Authors Alaric W. D'Souza, Robert F. Potter, Meghan Wallace, Angela Shupe, Sanket Patel, Xiaoqing Sun, Danish Gul, Jennie H. Kwon, Saadia Andleeb, Carey-Ann D. Burnham, and Gautam Dantas ARTICLE https://doi.org/10.1038/s41467-019-12563-1 OPEN Spatiotemporal dynamics of multidrug resistant bacteria on intensive care unit surfaces Alaric W. D’Souza 1,8, Robert F. Potter1,8, Meghan Wallace2, Angela Shupe2, Sanket Patel1,2, Xiaoqing Sun1,2, Danish Gul3, Jennie H. Kwon4, Saadia Andleeb3*, Carey-Ann D. Burnham2,4,5,6* & Gautam Dantas 1,2,5,7* Bacterial pathogens that infect patients also contaminate hospital surfaces. These con- taminants impact hospital infection control and epidemiology, prompting quantitative 1234567890():,; examination of their transmission dynamics. Here we investigate spatiotemporal and phy- logenetic relationships of multidrug resistant (MDR) bacteria on intensive care unit surfaces from two hospitals in the United States (US) and Pakistan collected over one year. MDR bacteria isolated from 3.3% and 86.7% of US and Pakistani surfaces, respectively, include common nosocomial pathogens, rare opportunistic pathogens, and novel taxa. Common nosocomial isolates are dominated by single lineages of different clones, are phenotypically MDR, and have high resistance gene burdens. Many resistance genes (e.g., blaNDM, blaOXA carbapenamases), are shared by multiple species and flanked by mobilization elements. We identify Acinetobacter baumannii and Enterococcus faecium co-association on multiple surfaces, and demonstrate these species establish synergistic biofilms in vitro. Our results highlight substantial MDR pathogen burdens in hospital built-environments, provide evidence for spatiotemporal-dependent transmission, and demonstrate potential mechanisms for multi- species surface persistence. 1 The Edison Family Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO, USA. 2 Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA. 3 Atta ur Rahman School of Applied Biosciences, National University of Sciences and Technology Islamabad, Islamabad, Pakistan. 4 Department of Medicine, Washington University School of Medicine, St. Louis, MO, USA. 5 Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO, USA. 6 Departments of Pediatrics, Washington University School of Medicine, St. Louis, MO, USA. 7 Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO, USA. 8These authors contributed equally: Alaric W. D’Souza, Robert F. Potter. *email: [email protected]; [email protected]; [email protected] NATURE COMMUNICATIONS | (2019) 10:4569 | https://doi.org/10.1038/s41467-019-12563-1 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-12563-1 lobal treatment of bacterial infections is increasingly transmission and protect vulnerable hospitalized patients25. Gcompromised by evolution and transmission of Additionally, such surveillance provides an opportunity to iden- multidrug-resistant organisms (MDROs) and their anti- tify and characterize potential emerging pathogens before they are biotic resistance genes (ARGs) between multiple habitats1. recognized in clinical infections13,26. Infections caused by MDROs are associated with increased To address the question of MDRO spatiotemporal dynamics mortality risk compared to infections by matched species sus- and persistence on healthcare surfaces we conducted a year-long ceptible isolates2–4. Through international travel, clonal expan- longitudinal study at a tertiary care hospital in Pakistan (PAK-H) sion, and promiscuous mobile genetic elements, MDROs and the where endemic ARG burden is high27–29. Differing resistance ARGs they harbor have rapidly swept across the globe1,5–12. mechanisms to last-resort carbapenem antibiotics have been Resistant infections cause over 23,000 annual deaths in the found in genetically similar Enterobacteriaceae strains and plas- United States of America (USA) and cost the economy over 55 mids isolated from hospitals in Pakistan and the USA30. billion dollars13. The annual global death toll from MDROs is at Accordingly, we included a matched tertiary care hospital in the least 700,000 people14. Improved surveillance and understanding USA (USA-H) as a comparison group. For our collections and of MDRO and ARG transmission are key factors in reducing subsequent analysis, we took an Eulerian approach by selecting these death tolls1,12. and measuring fixed hospital surfaces over time to understand Hospitalized patients are more vulnerable to bacterial infec- bacterial contamination dynamics. This approach allows us to tions than the general population15, and healthcare-associated leverage collection time information and surface spatial infor- infections (HAIs) acutely threaten patient safety worldwide16,17. mation to draw epidemiological insights. In both hospitals, we The “ESKAPE” pathogens, named by the Infectious Disease sampled four intensive care unit (ICU) rooms with five surfaces Society of America, are common causes of HAIs and the most in each room (Fig. 1). We collected surface swabs every other common MDROs18. These include the gram-positive micro- week for 3 months, and again at 6 months, and at 1 year, for a organisms Enterococcus spp. and Staphylococcus aureus, and the total of 180 samples per hospital. We identified high burdens of gram-negative microorganisms Klebsiella pneumoniae, Acineto- known MDROs on PAK-H ICU surfaces including ESKAPE bacter baumannii, Pseudomonas aeruginosa, and Enterobacter pathogens and novel taxa31,32. This investigation is the first to spp18. These ESKAPE pathogens can be acquired while hospita- show such widespread contamination with multidrug-resistant, lized, but some patients may be colonized or infected prior to extensively drug-resistant, and pan-drug-resistant bacteria in hospital admission19. Patients harboring these putative pathogens Pakistan. We found evidence that bacteria are non-randomly can transmit these bacteria to healthcare workers, other patients, distributed on hospital surfaces with respect to both space and medical equipment, and hospital surfaces19, but the relative time, and we used this information to narrow possible con- contribution of this contamination route compared to other tamination routes. We found cross-contamination of MDRO routes in unknown. The presence of these microorganisms on clones both across different surfaces within rooms, as well as surfaces in healthcare settings is a local and global public health between rooms at the same sampling time-points. From our concern20. Some putatively pathogenic strains of bacteria persist results, it is likely that bacteria are seeded to hospital surfaces for months on hospital surfaces, and they may even survive from diverse human and/or environmental reservoirs in a time- surface decontamination efforts, partly aided by biofilm forma- dependent manner. These seedings result in waves of con- tion21–24. Though studies clearly demonstrate that bacterial tamination that are often, but not always, restricted to a single pathogens exist on hospital surfaces, key knowledge gaps exist collection time. We show high numbers of ARGs are shared regarding the levels, types, and dynamics of contamination in between common nosocomial pathogens and rarer bacterial hospitals from different geographies15,19. Specifically, there is a species, including several novel taxa, which are close phylogenetic lack of information on the spatial, temporal, and phylogenetic relatives to nosocomial pathogens. Co-association analysis of A. relationships between different bacterial taxa on surfaces from baumannii and Enterococcus faecium led us to identify synergistic countries endemic for a high burden of ARGs. This information biofilm formation between these two ESKAPE pathogens. This gap is especially true for physical colocalization and horizontal discovery points to a possible explanation for multi-species bac- gene transfer between clinically relevant ESKAPE pathogens and terial persistence on hospital surfaces. Longitudinal persistence of benign environmental bacteria. these high-impact pathogenic species alongside highly resistant Monitoring high contact surfaces for clinically relevant bacteria classically identified as “environmental” paints a con- pathogenic bacteria and understanding the dynamics of their cerning picture of hospital surface contamination. These results persistence and spread is one approach to thwart MDRO lay the groundwork for future surveillance efforts and infection Longitudinal sampling of ICU surfaces For each ICU room in each collection in the United States and Pakistan Surfaces Swab each Every other week for 3 mo 6 mo 1 yr surface ON OFF Light switch Selective culture Nurse call button Sink handle Per country Bedside rail ×4 Per collection Foam dispenser MALDI-TOF MS and isolate sequencing Fig. 1 Overview of sample collection and processing. Samples were collected from surfaces longitudinally over the course of 1 year from PAK-H ICU and USA-H
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