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Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera

PURPOSE: We have previously shown that invasive strains of Pseudomonas aeruginosa exploit the robust neutrophil response to form biofilms on contact lens surfaces and invade the corneal epithelium. The present study investigated the ability of multiple bacterial genera, all commonly recovered during...

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Autores principales: Patel, Naiya B., Hinojosa, Jorge A., Zhu, Meifang, Robertson, Danielle M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Molecular Vision 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5800429/
https://www.ncbi.nlm.nih.gov/pubmed/29422767
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author Patel, Naiya B.
Hinojosa, Jorge A.
Zhu, Meifang
Robertson, Danielle M.
author_facet Patel, Naiya B.
Hinojosa, Jorge A.
Zhu, Meifang
Robertson, Danielle M.
author_sort Patel, Naiya B.
collection PubMed
description PURPOSE: We have previously shown that invasive strains of Pseudomonas aeruginosa exploit the robust neutrophil response to form biofilms on contact lens surfaces and invade the corneal epithelium. The present study investigated the ability of multiple bacterial genera, all commonly recovered during contact lens–related infectious events, to adhere to and form biofilms on contact lens surfaces in the presence of neutrophils. METHODS: Five reference strains from the American Type Culture Collection were used: P. aeruginosa, Serratia marcescens, Stenotrophomonas maltophilia, Staphylococcus aureus, and Staphylococcus epidermidis. Each bacterial strain was incubated overnight with or without stimulated human neutrophils in the presence of an unworn contact lens. Standard colony counts and laser scanning confocal microscopy of BacLight-stained contact lenses were used to assess bacterial viability. Three-dimensional modeling of lens-associated biofilms with Imaris software was used to determine the biofilm volume. Lenses were further examined using scanning electron microscopy. RESULTS: Less than 1% of the starting inoculum adhered to the contact lens surface incubated with bacteria alone. There were no differences in adhesion rates to contact lens surfaces between bacteria in the absence of neutrophils for either the Gram-negative or Gram-positive test strains. Bacterial adhesion to contact lens surfaces was accelerated in the presence of human neutrophils for all test strains. This effect was least evident with S. epidermidis. There was also an increase in the number of viable bacteria recovered from contact lens surfaces (p<0.001 for the Gram-negative and Gram-positive test strains, respectively) and in biofilm volume (p<0.001 for the Gram-negative test strains, p = 0.005 for S. aureus). CONCLUSIONS: These results show that in addition to P. aeruginosa, other bacteria commonly encountered during contact lens wear possess the capacity to utilize neutrophil-derived cellular debris to facilitate colonization of the lens surface. These data suggest that this phenomenon is conserved among multiple genera. Thus, during contact lens wear, the presence of inflammation and the accumulation of neutrophil debris under the posterior lens surface likely contribute to colonization of the lens. Further studies are needed to correlate these findings with risk for infection in an animal model.
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spelling pubmed-58004292018-02-08 Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera Patel, Naiya B. Hinojosa, Jorge A. Zhu, Meifang Robertson, Danielle M. Mol Vis Research Article PURPOSE: We have previously shown that invasive strains of Pseudomonas aeruginosa exploit the robust neutrophil response to form biofilms on contact lens surfaces and invade the corneal epithelium. The present study investigated the ability of multiple bacterial genera, all commonly recovered during contact lens–related infectious events, to adhere to and form biofilms on contact lens surfaces in the presence of neutrophils. METHODS: Five reference strains from the American Type Culture Collection were used: P. aeruginosa, Serratia marcescens, Stenotrophomonas maltophilia, Staphylococcus aureus, and Staphylococcus epidermidis. Each bacterial strain was incubated overnight with or without stimulated human neutrophils in the presence of an unworn contact lens. Standard colony counts and laser scanning confocal microscopy of BacLight-stained contact lenses were used to assess bacterial viability. Three-dimensional modeling of lens-associated biofilms with Imaris software was used to determine the biofilm volume. Lenses were further examined using scanning electron microscopy. RESULTS: Less than 1% of the starting inoculum adhered to the contact lens surface incubated with bacteria alone. There were no differences in adhesion rates to contact lens surfaces between bacteria in the absence of neutrophils for either the Gram-negative or Gram-positive test strains. Bacterial adhesion to contact lens surfaces was accelerated in the presence of human neutrophils for all test strains. This effect was least evident with S. epidermidis. There was also an increase in the number of viable bacteria recovered from contact lens surfaces (p<0.001 for the Gram-negative and Gram-positive test strains, respectively) and in biofilm volume (p<0.001 for the Gram-negative test strains, p = 0.005 for S. aureus). CONCLUSIONS: These results show that in addition to P. aeruginosa, other bacteria commonly encountered during contact lens wear possess the capacity to utilize neutrophil-derived cellular debris to facilitate colonization of the lens surface. These data suggest that this phenomenon is conserved among multiple genera. Thus, during contact lens wear, the presence of inflammation and the accumulation of neutrophil debris under the posterior lens surface likely contribute to colonization of the lens. Further studies are needed to correlate these findings with risk for infection in an animal model. Molecular Vision 2018-01-31 /pmc/articles/PMC5800429/ /pubmed/29422767 Text en Copyright © 2018 Molecular Vision. http://creativecommons.org/licenses/by-nc-nd/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited, used for non-commercial purposes, and is not altered or transformed.
spellingShingle Research Article
Patel, Naiya B.
Hinojosa, Jorge A.
Zhu, Meifang
Robertson, Danielle M.
Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title_full Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title_fullStr Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title_full_unstemmed Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title_short Acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
title_sort acceleration of the formation of biofilms on contact lens surfaces in the presence of neutrophil-derived cellular debris is conserved across multiple genera
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5800429/
https://www.ncbi.nlm.nih.gov/pubmed/29422767
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