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Biomedicines
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Biofilms in Wounds: New Advances in Therapy and in Healing...
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Biofilms in Wounds: New Advances in Therapy and in Healing Management

A special issue of Biomedicines (ISSN 2227-9059). This special issue belongs to the section "Molecular and Translational Medicine".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 28007

Special Issue Editors

Dr. Célia Fortuna Rodrigues

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Guest Editor
1. Associate Laboratory i4HB—Institute for Health and Bioeconomy, University Institute of Health Sciences—CESPU, 4585-116 Gandra, Portugal
2. ALiCE—Associate Laboratory in Chemical Engineering, Faculty of Engineering, LEPABE—Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal
Interests: biofilms; Candida; AMR; fungal infection; polymicrobial biofilms; alternatives to antifungals
Special Issues, Collections and Topics in MDPI journals
Dr. Karishma Kaushik

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Guest Editor
Institute of Bioinformatics and Biotechnology, Savitribai Phule Pune University (University of Pune), Ganeshkhind Rd, Ganeshkhind, Pune, Maharashtra 411007, India
Interests: wounds; biofilms; human-relevant; animal alternatives; polymicrobial
Dr. Caitlin Light

E-Mail Website
Co-Guest Editor
Biology Department, Binghamton University, Binghamton, NY 13902, USA
Interests: biofilm development, biofilm dispersion, bacterial signaling, outer membrane vesicles, virulence and pathogenesis

Special Issue Information

Dear Colleagues,

Biofilm is the predominant mode of life for bacteria and yeasts and is presently implicated in numerous human diseases. In fact, the majority of non-healing wounds contain biofilms, contributing to the high global cost of chronic wounds. Non-healing wounds with biofilms have a low-grade and persistent inflammatory response, which leads to impaired epithelialization and granulation tissue formation, and reduced susceptibility to antimicrobial agents. Furthermore, a compromised host defense severely delays the healing of wounds in patients, contributing to infection.

Therefore, reducing the biofilm’s presence in wounds is, indeed, a critical element of effective wound care. Strategies to manage biofilm and encourage progression to wound healing are urgently needed.

We warmly welcome you to join us in this effort. Reviews or original research articles are most welcome. We look forward to receiving your contributions.

Dr. Célia Fortuna Rodrigues
Dr. Caitlin Light
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Biomedicines is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • antimicrobial therapy
  • phage therapy
  • anti-biofilm technologies
  • acute and chronic wound management
  • dressing technologies

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Published Papers (5 papers)

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Editorial

Jump to: Research, Review

2 pages, 172 KiB  
Editorial
Biofilms in Wounds: New Advances in Therapy and in Healing Management
by Célia F. Rodrigues, Karishma S. Kaushik and Caitlin Light
Biomedicines 2021, 9(2), 193; https://doi.org/10.3390/biomedicines9020193 - 16 Feb 2021
Cited by 2 | Viewed by 1808
Abstract
Biofilms are the major way of life for both bacteria and fungi [...] Full article
(This article belongs to the Special Issue Biofilms in Wounds: New Advances in Therapy and in Healing Management)

Research

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20 pages, 6683 KiB  
Article
Thymoquinone-Loaded Polymeric Films and Hydrogels for Bacterial Disinfection and Wound Healing
by Anika Haq, Suneel Kumar, Yong Mao, Francois Berthiaume and Bozena Michniak-Kohn
Biomedicines 2020, 8(10), 386; https://doi.org/10.3390/biomedicines8100386 - 28 Sep 2020
Cited by 15 | Viewed by 3801
Abstract
The purpose of this study was to synthesize and characterize novel biocompatible topical polymeric film and hydrogel systems that have the potential to deliver the antibacterial agent thymoquinone (TQ) directly to the skin target site to manage the local wound infection and thereby [...] Read more.
The purpose of this study was to synthesize and characterize novel biocompatible topical polymeric film and hydrogel systems that have the potential to deliver the antibacterial agent thymoquinone (TQ) directly to the skin target site to manage the local wound infection and thereby wound healing. The polyvinyl pyrrolidone (PVP) matrix-type films containing TQ were prepared by the solvent casting method. In vitro skin permeation studies on human cadaver skin produced a mean flux of 2.3 µg TQ/cm2/h. Human keratinocyte monolayers subjected to a scratch wound (an in vitro wound healing assay) showed 85% wound closure at day 6 in the TQ group (100 ng/mL TQ) as compared to 50% in the vehicle control group (p = 0.0001). In a zone-of-inhibition (ZOI) assay, TQ-containing films and hydrogels completely wiped out Staphylococcus aureus in 10 cm diameter Tryptic Soy Agar plates while 500 µg/mL gentamicin containing filters gave 10 mm of ZOI. In an ex vivo model, TQ-containing films eradicated bacterial colonization on human cadaver skin. Furthermore, in a full-thickness wound infection model in mice, TQ-containing films showed significant activity in controlling Staphylococcus aureus infection, thereby disinfecting the skin wound. In summary, TQ-containing PVP films and hydrogels developed in this study have the potential to treat and manage wound infections. Full article
(This article belongs to the Special Issue Biofilms in Wounds: New Advances in Therapy and in Healing Management)
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Graphical abstract

Graphical abstract
Full article ">Figure 1
<p>Flow chart depicting the experimental design for in-vivo evaluation of TQ film in a mouse model of bacterial infection. The number of mice used in each experimental group and the timeline for treatment. The time of treatment and sample collection of bacteria (red letters) is shown for each group (green letter indicates on TQ film treatment on day 10).</p> Full article ">Figure 2
<p>Physicochemical characterization of TQ films. (<b>A</b>) FTIR spectrum of TQ pure drug, PVP, physical mixture of drug and polymer, freshly prepared films containing drug and polymer, stored films containing drug and polymer; (<b>B</b>) Control films (i), Field emission scanning electron microscopic (FESEM) images showing the surface morphology of control film (ii–iii) at different magnifications (scale bar = 100 µm), and (<b>C</b>) TQ films (i), FESEM images showing the surface morphology of TQ films (ii–iii) at different magnifications (scale bar = 100 µm).</p> Full article ">Figure 3
<p>Rheological characterization of TQ hydrogel formulations (F1–F10). (<b>A</b>) Oscillation frequency sweep data. The elastic modulus (i); The viscous modulus (ii) were plotted against angular frequency. TQ permeation and skin deposition from film and gel formulations (<b>B</b>). TQ permeation profile for different hydrogel formulations (i). Time points were measured at 1, 2, 3, 4, 5, 6, and 8 h. Each point represents the five experiments; TQ permeation from film formulation across human cadaver skin (<span class="html-italic">n</span> = 5) (ii); Amount of TQ detected after 8 h in human cadaver skin (<span class="html-italic">n</span> = 5) using different TQ hydrogel formulations (iii).</p> Full article ">Figure 4
<p>The cytocompatibility study of TQ film. Cell viability of TQ film with HDF and HaCaT cells using alamarBlue<sup>®</sup> assay.</p> Full article ">Figure 5
<p>Bacterial inhibition study. (<b>A</b>) Inhibition of bacterial growth on agar plate by Control negative (i); Gentamicin positive control 50 µg/mL (ii) right upper and 500 µg/mL (ii) right lower; Control film (iii); TQ hydrogel (iv) and TQ film (v) against <span class="html-italic">S. aureus</span>; (<b>B</b>) Ex vivo antibacterial activity by Control (i); Control film (ii); Gentamicin sulfate USP, 0.1% marketed cream (iii); TQ hydrogel (iv); TQ film (v) and Log of bacterial reduction with different treatment groups (vi). Data represent of four replicates. *** <span class="html-italic">p</span> ≤ 0.001 and ^^^ <span class="html-italic">p</span> ≤ 0.05.</p> Full article ">Figure 6
<p>Effect of TQ treatment on the wound healing of human fibroblasts. (<b>A</b>) Representative micrographs (10×) from fibroblast cell migration including different treatment groups (Control, 1 ng/mL, and 100 ng/mL of TQ) showing the original wound and the wound after 12 h and 24 h; (<b>B</b>) Quantitative analysis of wound closure as a function of time. The wound area was determined as the wound area at a given time relative to the original wound area (<span class="html-italic">n</span> = 6). ** <span class="html-italic">p</span> &lt; 0.01 and *** <span class="html-italic">p</span> &lt; 0.001 (Control vs. 100 ng/mL) and ^ <span class="html-italic">p</span> &lt; 0.05 (Control vs. 1 ng/mL); (<b>C</b>) Quantitative measurement of cell number migrating in the corresponding scratched wound areas at 24 h in the different treatment groups (<span class="html-italic">n</span> = 6). *** <span class="html-italic">p</span> &lt; 0.001 (100 ng/mL vs. control and 1 ng/mL).</p> Full article ">Figure 7
<p>Effect of TQ treatment on the wound healing of keratinocytes using scratch assay. (<b>A</b>) Representative micrographs (10×) from Control (+Ve), Control, 1 ng/mL, and 100 ng/mL of TQ showing the original wound at day 0 and the wounds after 3 and 6 days of keratinocyte cell migration; (<b>B</b>) Quantitative analysis of wound closure as a function of time. The wound area was determined as the wound area at a given time relative to the original wound area at day 0 (<span class="html-italic">n</span> = 5–6). *** <span class="html-italic">p</span> &lt; 0.001 (Control vs. Control + Ve), ^^ <span class="html-italic">p</span> &lt; 0.01 (Control vs. 1 ng/mL) and ### <span class="html-italic">p</span> &lt; 0.001 (Control vs. 100 ng/mL).</p> Full article ">Figure 8
<p>Antibacterial effects of TQ films on full-thickness skin wounds infected with <span class="html-italic">S. aureus</span>. (<b>A</b>) Photographs of skin wounds with different treatments over 21 days. The wounds were infected with bacteria as shown above as a pale biofilm in the bacteria wound group and other related groups. Scale bar = 1 cm. (<b>B</b>) Log of bacterial reduction at each timepoint up to 7 days assessed in different experimental groups. *** <span class="html-italic">p</span> &lt; 0.001 (Bacterial wound vs. TQ Film) and ^^^ <span class="html-italic">p</span> &lt; 0.001 (Bacterial wound vs. Gentamicin). (<b>C</b>) Percentage of wound closure as a function of time in all experimental groups at different time points post-wounding and treatments. ** <span class="html-italic">p</span> &lt; 0.01 (Control wound vs. Control Film) and # <span class="html-italic">p</span> &lt; 0.05 (Control Film vs. Gentamicin).</p> Full article ">
10 pages, 4290 KiB  
Article
Organo-Selenium-Containing Polyester Bandage Inhibits Bacterial Biofilm Growth on the Bandage and in the Wound
by Phat Tran, Tyler Enos, Keaton Luth, Abdul Hamood, Coby Ray, Kelly Mitchell and Ted W. Reid
Biomedicines 2020, 8(3), 62; https://doi.org/10.3390/biomedicines8030062 - 17 Mar 2020
Cited by 9 | Viewed by 3275
Abstract
The dressing material of a wound plays a key role since bacteria can live in the bandage and keep re-infecting the wound, thus a bandage is needed that blocks biofilm in the bandage. Using an in vivo wound biofilm model, we examined the [...] Read more.
The dressing material of a wound plays a key role since bacteria can live in the bandage and keep re-infecting the wound, thus a bandage is needed that blocks biofilm in the bandage. Using an in vivo wound biofilm model, we examined the effectiveness of an organo-selenium (OS)-coated polyester dressing to inhibit the growth of bacteria in a wound. Staphylococcus aureus (as well as MRSA, Methicillin resistant Staph aureus), Stenotrophomonas maltophilia, Enterococcus faecalis, Staphylococcus epidermidis, and Pseudomonas aeruginosa were chosen for the wound infection study. All the bacteria were enumerated in the wound dressing and in the wound tissue under the dressing. Using colony-forming unit (CFU) assays, over 7 logs of inhibition (100%) was found for all the bacterial strains on the material of the OS-coated wound dressing and in the tissue under that dressing. Confocal laser scanning microscopy along with IVIS spectrum in vivo imaging confirmed the CFU results. Thus, the dressing acts as a reservoir for a biofilm, which causes wound infection. The same results were obtained after soaking the dressing in PBS at 37 °C for three months before use. These results suggest that an OS coating on polyester dressing is both effective and durable in blocking wound infection. Full article
(This article belongs to the Special Issue Biofilms in Wounds: New Advances in Therapy and in Healing Management)
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Figure 1

Figure 1
<p>Graph of the colony-forming units of (<b>A</b>) <span class="html-italic">Staphylococcus aureus</span> GFP AH133, (<b>B</b>) <span class="html-italic">Stenotrophomonas maltophilia</span> ATCC<sup>®</sup> 53199™, (<b>C</b>) <span class="html-italic">Pseudomonas aeruginosa</span> PAO1 GFP, (<b>D</b>) <span class="html-italic">Enterococcus faecalis</span> GFP, (<b>E</b>) Methicillin-resistant <span class="html-italic">Staphylococcus aureus</span> CI 1, (<b>F</b>) Methicillin-resistant <span class="html-italic">Staphylococcus aureus</span> CI 2, and (<b>G</b>) <span class="html-italic">Staphylococcus epidermidis</span> CI biofilms formed on untreated polyester and 1% Se-AAEMA polyester. Values represent the means of triplicate experiments ± SEM. A two-tailed unpaired t test was used to determine statistical significance. Untreated polyester has AAEMA but no selenium.</p> Full article ">Figure 2
<p>In Vitro study. Representative confocal laser scanning microscopy images of (<b>A</b>) <span class="html-italic">Staphylococcus aureus</span> GFP AH133, (<b>B</b>) <span class="html-italic">Pseudomonas aeruginosa</span> PAO1 GFP, and (<b>C</b>) <span class="html-italic">Enterococcus faecalis GFP</span> biofilm formed on untreated polyester and 1% Se-AAEMA polyester. Untreated polyester has AAEMA but no selenium. (<b>D</b>–<b>F</b>) are the same samples as those above however they have Se-AAEMA. As seen all the bacteria are eliminated. The bar is 200 μm.</p> Full article ">Figure 3
<p>Graph of the colony-forming units of (<b>A</b>) <span class="html-italic">Staphylococcus aureus</span> GFP AH133, (<b>B</b>) <span class="html-italic">Pseudomonas aeruginosa</span> PAO1 GFP, (<b>C</b>) Methicillin-resistant <span class="html-italic">Staphylococcus aureus</span> CI 1, and (<b>D</b>) Methicillin-resistant <span class="html-italic">Staphylococcus aureus</span> CI 2 biofilms formed on the polyester dressings and in the tissue under the polyester dressings on a mouse wound. Values represent the means of six replicate experiments ± SEM. A two-tailed unpaired t test was used to determine statistical significance. Untreated polyester has AAEMA but no selenium.</p> Full article ">Figure 4
<p>Mouse wounds after 5 days. Representative confocal laser scanning microscopy images of (<b>A</b>) <span class="html-italic">Staphylococcus aureus</span> GFP AH133 with untreated polyester showing bacteria in the AAEMA bandage, and (<b>B</b>) is the same except it is with a Se-AAEMA bandage, while (<b>E</b>) is the tissue under bandage (<b>A</b>), and (<b>F</b>) is the tissue under bandage (<b>B</b>). (<b>C</b>) is <span class="html-italic">Pseudomonas aeruginosa</span> PAO1 GFP biofilms formed on the AAEMA treated polyester dressings and (<b>D</b>) is the same as (<b>A</b>) except it is with the SeAAEMA treated dressing. (<b>G</b>) is the tissue under the polyester dressings (<b>A</b>), and (<b>H</b>) is the tissue under the SeAAEMA bandage (<b>D</b>). Bar is 100 μm.</p> Full article ">Figure 5
<p>Graphs of the colony-forming units recovered from the effect of AAEMA and SeAAEMA coated polyester dressing (<b>A</b>) <span class="html-italic">S. aureus</span> Lux Xen29 and (<b>B</b>) <span class="html-italic">P. aeruginosa</span> Lux Xen5 in the polyester dressings and the mouse wound tissue. Untreated polyester has AAEMA but no selenium.</p> Full article ">Figure 6
<p>Representative IVIS in vivo live images of (<b>A</b>) <span class="html-italic">S. aureus</span> Lux Xen29 under AAEMA polyester dressing and (<b>B</b>) Se-AAEMA polyester dressing. (<b>C</b>) <span class="html-italic">P. aeruginosa</span> Lux Xen5 biofilms formed under the AAEMA polyester dressings and (<b>D</b>) the Se-AAEMA polyester dressing.</p> Full article ">Figure 7
<p>Stability study of bandage after one month in PBS at 37 °C. The inhibitory effect of the organo-selenium coating is long-lasting against <span class="html-italic">Staphylococcus aureus</span> GFP AH133 biofilms formed on untreated polyester and 1% Se-AAEMA polyester, which were previously soaked in 1× PBS (pH = 7.4) for three months. Values represent the means of quadruplicate experiments ± SEM. (<b>A</b>) two-tailed unpaired t test was used to determine statistical significance. Representative confocal laser scanning microscopy images of (<b>B</b>) <span class="html-italic">Staphylococcus aureus</span> GFP AH133 biofilms formed on untreated polyester and (<b>C</b>) 1% Se-AAEMA polyester, which were previously soaked in 1× PBS (pH = 7.4) for three months. Untreated polyester has AAEMA but no selenium. Bar is 200 m.</p> Full article ">

Review

Jump to: Editorial, Research

26 pages, 417 KiB  
Review
Recent Advances in Non-Conventional Antimicrobial Approaches for Chronic Wound Biofilms: Have We Found the ‘Chink in the Armor’?
by Snehal Kadam, Saptarsi Shai, Aditi Shahane and Karishma S Kaushik
Biomedicines 2019, 7(2), 35; https://doi.org/10.3390/biomedicines7020035 - 30 Apr 2019
Cited by 62 | Viewed by 9782
Abstract
Chronic wounds are a major healthcare burden, with huge public health and economic impact. Microbial infections are the single most important cause of chronic, non-healing wounds. Chronic wound infections typically form biofilms, which are notoriously recalcitrant to conventional antibiotics. This prompts the need [...] Read more.
Chronic wounds are a major healthcare burden, with huge public health and economic impact. Microbial infections are the single most important cause of chronic, non-healing wounds. Chronic wound infections typically form biofilms, which are notoriously recalcitrant to conventional antibiotics. This prompts the need for alternative or adjunct ‘anti-biofilm’ approaches, notably those that account for the unique chronic wound biofilm microenvironment. In this review, we discuss the recent advances in non-conventional antimicrobial approaches for chronic wound biofilms, looking beyond standard antibiotic therapies. These non-conventional strategies are discussed under three groups. The first group focuses on treatment approaches that directly kill or inhibit microbes in chronic wound biofilms, using mechanisms or delivery strategies distinct from antibiotics. The second group discusses antimicrobial approaches that modify the biological, chemical or biophysical parameters in the chronic wound microenvironment, which in turn enables the disruption and removal of biofilms. Finally, therapeutic approaches that affect both, biofilm bacteria and microenvironment factors, are discussed. Understanding the advantages and limitations of these recent approaches, their stage of development and role in biofilm management, could lead to new treatment paradigms for chronic wound infections. Towards this end, we discuss the possibility that non-conventional antimicrobial therapeutics and targets could expose the ‘chink in the armor’ of chronic wound biofilms, thereby providing much-needed alternative or adjunct strategies for wound infection management. Full article
(This article belongs to the Special Issue Biofilms in Wounds: New Advances in Therapy and in Healing Management)
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Graphical abstract

Graphical abstract
Full article ">
31 pages, 2227 KiB  
Review
Current Status of In Vitro Models and Assays for Susceptibility Testing for Wound Biofilm Infections
by Tania F. Bahamondez-Canas, Lara A. Heersema and Hugh D. C. Smyth
Biomedicines 2019, 7(2), 34; https://doi.org/10.3390/biomedicines7020034 - 30 Apr 2019
Cited by 49 | Viewed by 8259
Abstract
Biofilm infections have gained recognition as an important therapeutic challenge in the last several decades due to their relationship with the chronicity of infectious diseases. Studies of novel therapeutic treatments targeting infections require the development and use of models to mimic the formation [...] Read more.
Biofilm infections have gained recognition as an important therapeutic challenge in the last several decades due to their relationship with the chronicity of infectious diseases. Studies of novel therapeutic treatments targeting infections require the development and use of models to mimic the formation and characteristics of biofilms within host tissues. Due to the diversity of reported in vitro models and lack of consensus, this review aims to provide a summary of in vitro models currently used in research. In particular, we review the various reported in vitro models of Pseudomonas aeruginosa biofilms due to its high clinical impact in chronic wounds and in other chronic infections. We assess advances in in vitro models that incorporate relevant multispecies biofilms found in infected wounds, such as P. aeruginosa with Staphylococcus aureus, and additional elements such as mammalian cells, simulating fluids, and tissue explants in an attempt to better represent the physiological conditions found at an infection site. It is hoped this review will aid researchers in the field to make appropriate choices in their proposed studies with regards to in vitro models and methods. Full article
(This article belongs to the Special Issue Biofilms in Wounds: New Advances in Therapy and in Healing Management)
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Graphical abstract

Graphical abstract
Full article ">Figure 1
<p>Number of publications per year with the word biofilms in the title of the article searched by Google Scholar. The labels indicate the dates where the evidence of biofilms in new tissues was published.</p> Full article ">Figure 2
<p>Stages of biofilm development: (1) Reversible attachment, (2) Irreversible attachment, (3) Maturation 1, (4) Maturation 2, and (5) Dispersion [<a href="#B76-biomedicines-07-00034" class="html-bibr">76</a>].</p> Full article ">Figure 3
<p>The heterogeneous susceptibility of bacterial biofilms to antibiotics [<a href="#B88-biomedicines-07-00034" class="html-bibr">88</a>].</p> Full article ">Figure 4
<p>Different systems for static growth of biofilm. (<b>A</b>) Colony biofilm model, (<b>B</b>) Calgary device lid, and (<b>C</b>) round bottom 96-well plate.</p> Full article ">Figure 5
<p>General schematics of the components of flow cell systems for biofilm formation.</p> Full article ">Figure 6
<p>General schematics of the components of biofilm reactors.</p> Full article ">
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