Vancomycin and maltodextrin affect structure and activity of <i>Staphylococcus aureus</i> biofilms

Kiamco, Mia Mae; Atçı, Erhan; Khan, Qaiser Farid; Mohamed, Abdelrhman; Renslow, Ryan; Abu-Lail, Nehal I.; Fransson, Boel A.; Call, Douglas R.; Beyenal, Haluk

doi:10.1002/bit.25681

Cited by 16 publications

(33 citation statements)

References 62 publications

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“…Increasing the concentration of maltodextrin up to 40 mM in combination with an e-scaffold did not increase biofilm elimination. This may be due to blockage of H 2 O 2 diffusion pathways through the biofilm matrix at higher concentrations of maltodextrin, since the relative diffusivity of an antimicrobial can decrease with increasing concentrations of maltodextrin, as observed previously4953.…”

Section: Discussionsupporting

confidence: 56%

“…It can also enhance H 2 O 2 entry into cells by “stretching” the lipid bilayer24. Further increasing the osmolarity of the medium with a hyperosmotic agent, however, can eventually cause blockage of the transportation pathway49. In addition, at higher osmolarities bacteria synthesize more osmolytes that protect the cells by impeding antimicrobial entry50.…”

mentioning

confidence: 99%

“…Based on our previous work with hyperosmotic agent treatments49 we hypothesized that operation of an e-scaffold in the presence of maltodextrin, a hyperosmotic agent, would be more effective against A. baumannii and S. aureus biofilms than treatment with either individual application alone. Maltodextrin is a product of hydrolyzed starch and is composed of sugars and polysaccharides.…”

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confidence: 99%

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Maltodextrin enhances biofilm elimination by electrochemical scaffold

Sultana

Call

Beyenal

2016

Sci Rep

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Electrochemical scaffolds (e-scaffolds) continuously generate low concentrations of H2O2 suitable for damaging wound biofilms without damaging host tissue. Nevertheless, retarded diffusion combined with H2O2 degradation can limit the efficacy of this potentially important clinical tool. H2O2 diffusion into biofilms and bacterial cells can be increased by damaging the biofilm structure or by activating membrane transportation channels by exposure to hyperosmotic agents. We hypothesized that e-scaffolds would be more effective against Acinetobacter baumannii and Staphylococcus aureus biofilms in the presence of a hyperosmotic agent. E-scaffolds polarized at −600 mVAg/AgCl were overlaid onto preformed biofilms in media containing various maltodextrin concentrations. E-scaffold alone decreased A. baumannii and S. aureus biofilm cell densities by (3.92 ± 0.15) log and (2.31 ± 0.12) log, respectively. Compared to untreated biofilms, the efficacy of the e-scaffold increased to a maximum (8.27 ± 0.05) log reduction in A. baumannii and (4.71 ± 0.12) log reduction in S. aureus biofilm cell densities upon 10 mM and 30 mM maltodextrin addition, respectively. Overall ~55% decrease in relative biofilm surface coverage was achieved for both species. We conclude that combined treatment with electrochemically generated H2O2 from an e-scaffold and maltodextrin is more effective in decreasing viable biofilm cell density.

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Section: Discussionsupporting

confidence: 56%

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confidence: 99%

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confidence: 99%

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Maltodextrin enhances biofilm elimination by electrochemical scaffold

Sultana

Call

Beyenal

2016

Sci Rep

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“…Additionally, the balance of water activity plays a critical role in a wide range of cellular and antibiotic functions and in mass transport in biofilms (31)(32)(33). A shift to a hyperosmotic environment challenges biofilm homeostasis, which in turn threatens the integrity of bacterial cellular membranes (34)(35)(36), improves antibiotic effectiveness (37), and exhausts the buffering capacity of bacterial cytoplasm, which may also result in a reduction in pH (38,39). Thus, combining a high concentration of antibiotics with a hyperosmotic agent offers an alternative treatment strategy for biofilm communities.…”

mentioning

confidence: 99%

“…Hyperosmotic concentrations of agents, such as medical-grade honey (48,49) and cadexomer iodine (50,51), have been considered for wound treatment. Recently, it was shown that hyperosmotic concentrations of maltodextrin increased the efficiency of vancomycin against S. aureus biofilms by reducing biofilm coverage, thickness, and diffusion distance, as well as by improving the DO concentration within the biofilm (37). To the best of our knowledge, the variation in DO concentration and pH in S. aureus biofilms that are treated with medical-grade honey or cadexomer iodine combined with vancomycin or ciprofloxacin has not been investigated.…”

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confidence: 99%

Hyperosmotic Agents and Antibiotics Affect Dissolved Oxygen and pH Concentration Gradients in Staphylococcus aureus Biofilms

Kiamco

Atçı

Mohamed

et al. 2017

Appl Environ Microbiol

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Biofilms on wound surfaces are treated topically with hyperosmotic agents, such as medical-grade honey and cadexomer iodine; in some cases, these treatments are combined with antibiotics. Tissue repair requires oxygen, and a low pH is conducive to oxygen release from red blood cells and epithelialization. We investigated the variation of dissolved oxygen concentration and pH with biofilm depth and the variation in oxygen consumption rates when biofilms are challenged with medical-grade honey or cadexomer iodine combined with vancomycin or ciprofloxacin. Dissolved oxygen and pH depth profiles in Staphylococcus aureus biofilms were measured using microelectrodes. The presence of cadexomer iodine with vancomycin or ciprofloxacin on the surface of the biofilm permitted a measurable concentration of oxygen at greater biofilm depths (101.6 Ϯ 27.3 m, P ϭ 0.02; and 155.5 Ϯ 27.9 m, P ϭ 0.016, respectively) than in untreated controls (30.1 m). Decreases in pH of ϳ0.6 and ϳ0.4 units were observed in biofilms challenged with medical-grade honey alone and combined with ciprofloxacin, respectively (P Ͻ 0.001 and 0.01, respectively); the number of bacteria recovered from biofilms was significantly reduced (1.26 log) by treatment with cadexomer iodine and ciprofloxacin (P ϭ 0.002) compared to the untreated control. Combining cadexomer iodine and ciprofloxacin improved dissolved oxygen concentration and penetration depth into the biofilm, while medical-grade honey was associated with a lower pH; not all treatments established a bactericidal effect in the time frame used in the experiments.IMPORTANCE Reports about using hyperosmotic agents and antibiotics against wound biofilms focus mostly on killing bacteria, but the results of these treatments should additionally be considered in the context of how they affect physiologically important parameters, such as oxygen concentration and pH. We confirmed that the combination of a hyperosmotic agent and an antibiotic results in greater dissolved oxygen and reduced pH within an S. aureus biofilm.

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Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress

Kiamco

Mohamed

Reardon

et al. 2018

Biotech & Bioengineering

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Biofilms alter their metabolism in response to environmental stress. This study explores the effect of a hyperosmotic agent–antibiotic treatment on the metabolism of Staphylococcus aureus biofilms through the use of nuclear magnetic resonance (NMR) techniques. To determine the metabolic activity of S. aureus, we quantified the concentrations of metabolites in spent medium using high-resolution NMR spectroscopy. Biofilm porosity, thickness, biovolume, and relative diffusion coefficient depth profiles were obtained using NMR microimaging. Dissolved oxygen concentration was measured to determine the availability of oxygen within the biofilm. Under vancomycin-only treatment, the biofilm communities switched to fermentation under anaerobic condition, as evidenced by high concentrations of formate (7.4 ± 2.7 mM), acetate (13.1 ± 0.9 mM), and lactate (3.0 ± 0.8 mM), and there was no detectable dissolved oxygen in the biofilm. In addition, we observed the highest consumption of pyruvate (0.19 mM remaining from an initial 40 mM concentration), the sole carbon source, under the vancomycin-only treatment. On the other hand, relative effective diffusion coefficients increased from 0.73 ± 0.08 to 0.88 ± 0.08 under vancomycin-only treatment but decreased from 0.71 ± 0.04 to 0.60 ± 0.07 under maltodextrin-only and from 0.73 ± 0.06 to 0.56 ± 0.08 under combined treatments. There was an increase in biovolume, from 2.5 ± 1 mm3 to 7 ± 1 mm3, under the vancomycin-only treatment, while the maltodextrin-only and combined treatments showed no significant change in biovolume over time. This indicated that physical biofilm growth was halted during maltodextrin-only and combined treatments.

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Vancomycin and maltodextrin affect structure and activity of Staphylococcus aureus biofilms

Cited by 16 publications

References 62 publications

Maltodextrin enhances biofilm elimination by electrochemical scaffold

Maltodextrin enhances biofilm elimination by electrochemical scaffold

Hyperosmotic Agents and Antibiotics Affect Dissolved Oxygen and pH Concentration Gradients in Staphylococcus aureus Biofilms

Structural and metabolic responses of Staphylococcus aureus biofilms to hyperosmotic and antibiotic stress

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