Delayed neutrophil recruitment allows nascent Staphylococcus aureus biofilm formation and immune evasion

Pettygrove, Brian A.; Kratofil, Rachel M.; Alhede, Morten; Jensen, Peter Østrup; Newton, Michelle; Qvortrup, Klaus; Pallister, Kyler B.; Bjarnsholt, Thomas; Kubes, Paul; Voyich, Jovanka M.; Stewart, Philip S.

doi:10.1016/j.biomaterials.2021.120775

Cited by 27 publications

(30 citation statements)

References 42 publications

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“…Previous and ongoing studies in our lab have utilized a time lapse imaging system to analyze interactions between human PMNs and surface adherent S. aureus (Ghimire et al, 2019 ; Pettygrove et al, 2021 ). Data were mined from two types of experiments that were performed to investigate the effects of PMN density and S. aureus aggregate size on the overall clearance of S. aureus from a glass surface.…”

Section: Resultsmentioning

confidence: 99%

“…Extensive time-lapse microscopy data of bacterial growth spanning an 8-h time frame and several corresponding treatment conditions were collected for each of the described experiments ( Figures 2 , 3 ). The overarching results and interpretation of these experiments will not be discussed at length here but are the subject of a separate manuscript (Pettygrove et al, 2021 ). For density experiments it was observed that a high concentration of PMNs was required to clear adherent S. aureus with the “medium” and “high” treatment conditions resulting in significant clearance of bacteria ( Figures 3A–C ).…”

Section: Resultsmentioning

confidence: 99%

“…Real-time CLSM non-invasively provides quantitative insight into the dynamics of living biofilms (Stewart et al, 2009 ; Davison et al, 2010 ; McLoon et al, 2011 ; Hung et al, 2013 ; Franklin et al, 2015 ; Ghimire et al, 2019 ; Pettygrove et al, 2021 ). Continued exploration in this area by our lab has yielded an abundance of time-lapse microscopy data that can inform the proper design of microscopy studies (Ghimire et al, 2019 ; Pettygrove et al, 2021 ). The data included are particularly suitable for assisting with the experimental design of studies investigating initial bacterial attachment, early biofilm formation, and biocidal treatments of bacteria in this stage.…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Experimental Designs to Study the Aggregation and Colonization of Biofilms by Video Microscopy With Statistical Confidence

et al. 2022

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The goal of this study was to quantify the variability of confocal laser scanning microscopy (CLSM) time-lapse images of early colonizing biofilms to aid in the design of future imaging experiments. To accomplish this a large imaging dataset consisting of 16 independent CLSM microscopy experiments was leveraged. These experiments were designed to study interactions between human neutrophils and single cells or aggregates of Staphylococcus aureus (S. aureus) during the initial stages of biofilm formation. Results suggest that in untreated control experiments, variability differed substantially between growth phases (i.e., lag or exponential). When studying the effect of an antimicrobial treatment (in this case, neutrophil challenge), regardless of the inoculation level or of growth phase, variability changed as a frown-shaped function of treatment efficacy (i.e., the reduction in biofilm surface coverage). These findings were used to predict the best experimental designs for future imaging studies of early biofilms by considering differing (i) numbers of independent experiments; (ii) numbers of fields of view (FOV) per experiment; and (iii) frame capture rates per hour. A spreadsheet capable of assessing any user-specified design is included that requires the expected mean log reduction and variance components from user-generated experimental results. The methodology outlined in this study can assist researchers in designing their CLSM studies of antimicrobial treatments with a high level of statistical confidence.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Experimental Designs to Study the Aggregation and Colonization of Biofilms by Video Microscopy With Statistical Confidence

et al. 2022

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“…Microorganisms embedded in biofilms show a drastically reduced susceptibility to antimicrobial agents (antibiotics and disinfectants), which is not only due to their well-known resistance mechanisms (including efflux, the enzymatic inactivation of the antibiotic and target modification), but is also related to the biofilm-specific tolerance mechanisms (including metabolic changes and reduced transport of antimicrobials into the biofilm) [37,38]. In addition, biofilm-associated microorganisms are not easily cleared by the immune system [39]. Biofilm formation on (implanted) medical devices is a well-known problem that has a substantial impact on morbidity and mortality [40].…”

Section: Understanding the Importance Of Biofilm Formation In Abdomin...mentioning

confidence: 99%

The Role of Abdominal Drain Cultures in Managing Abdominal Infections

et al. 2022

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Intra-abdominal infections (IAI) are common in hospitalized patients, both in and outside of the intensive care unit. Management principles include antimicrobial therapy and source control. Typically, these infections are polymicrobial, and intra-operative samples will guide the targeted antimicrobial therapy. Although the use of prophylactic abdominal drains in patients undergoing abdominal surgery is decreasing, the use of drains to treat IAI, both in surgical and non-surgical strategies for abdominal infection, is increasing. In this context, samples from abdominal drains are often used to assist in antimicrobial decision making. In this narrative review, we provide an overview of the current role of abdominal drains in surgery, discuss the importance of biofilm formation in abdominal drains and the mechanisms involved, and review the clinical data on the use of sampling these drains for diagnostic purposes. We conclude that biofilm formation and the colonization of abdominal drains is common, which precludes the use of abdominal fluid to reliably diagnose IAI and identify the pathogens involved. We recommend limiting the use of drains and, when present, avoiding routine microbiological sampling.

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Biofilm Microenvironment‐Responsive Self‐Assembly Nanoreactors for All‐Stage Biofilm Associated Infection through Bacterial Cuproptosis‐like Death and Macrophage Re‐Rousing

Mei

Wang

et al. 2023

Advanced Materials

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Bacterial biofilm‐associated infections (BAIs) are the leading cause of prosthetic implant failure. The dense biofilm structure prevents antibiotic penetration, while the highly acidic and H2O2‐rich biofilm microenvironment (BME) dampens the immunological response of antimicrobial macrophages. Conventional treatments that fail to consistently suppress escaping planktonic bacteria from biofilm result in refractory recolonization, allowing BAIs to persist. Herein, a BME‐responsive copper‐doped polyoxometalate clusters (Cu‐POM) combination with mild photothermal therapy (PTT) and macrophage immune re‐rousing for BAI eradication at all stages is proposed. The self‐assembly of Cu‐POM in BME converts endogenous H2O2 to toxic ·OH through chemodynamic therapy (CDT) and generates a mild PTT effect to induce bacterial metabolic exuberance, resulting in loosening the membrane structure of the bacteria, enhancing copper transporter activity and increasing intracellular Cu‐POM flux. Metabolomics reveals that intracellular Cu‐POM overload restricts the TCA cycle and peroxide accumulation, promoting bacterial cuproptosis‐like death. CDT re‐rousing macrophages scavenge planktonic bacteria escaping biofilm disintegration through enhanced chemotaxis and phagocytosis. Overall, BME‐responsive Cu‐POM promotes bacterial cuproptosis‐like death via metabolic interference, while also re‐rousing macrophage immune response for further planktonic bacteria elimination, resulting in all‐stage BAI clearance and providing a new reference for future clinical application.

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Delayed neutrophil recruitment allows nascent Staphylococcus aureus biofilm formation and immune evasion

Cited by 27 publications

References 42 publications

Experimental Designs to Study the Aggregation and Colonization of Biofilms by Video Microscopy With Statistical Confidence

Experimental Designs to Study the Aggregation and Colonization of Biofilms by Video Microscopy With Statistical Confidence

The Role of Abdominal Drain Cultures in Managing Abdominal Infections

Biofilm Microenvironment‐Responsive Self‐Assembly Nanoreactors for All‐Stage Biofilm Associated Infection through Bacterial Cuproptosis‐like Death and Macrophage Re‐Rousing

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