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The Role of Biofilms in the Development and Dissemination of...
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The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry

A special issue of Foods (ISSN 2304-8158). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (31 January 2019) | Viewed by 46080

Printed Edition Available!
A printed edition of this Special Issue is available here.

Special Issue Editors

Dr. Efstathios Giaouris

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Guest Editor
Laboratory of Food Microbiology and Hygiene, Department of Food Science and Nutrition, School of the Environment, University of the Aegean, 81400 Myrina, Greece
Interests: biofilms; antimicrobial resistance and tolerance; foodborne bacterial pathogens; virulence and pathogenesis; disinfection; novel (green) antimicrobials; food hygiene and safety; quorum sensing; intercellular interactions; bacterial stress adaptation
Special Issues, Collections and Topics in MDPI journals
Dr. Manuel Simões

grade E-Mail Website
Co-Guest Editor
LEPABE, Department of Chemical Engineering, Faculty of Engineering, University of Porto, Rua Roberto Frias, s/n, 4200-465 Porto, Portugal
Interests: antimicrobial agents; emerging antimicrobial strategies; antimicrobial resistance; biofilms; plant secondary metabolites
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Florence Dubois-Brissonnet

E-Mail Website
Co-Guest Editor
AgroParisTech, Dépt. Sciences et Procédés des Aliments et des Bioproduits, Institut MICALIS (UMR INRA/AgroParisTech) - Equipe Bioadhésion, Biofilm et Hygiène des Matériaux, Centre INRA de Jouy-en Josas, Batiment 440, R-2, Domaine de Vilvert, 78350 Jouy-en-Josas, France

Special Issue Information

Dear Colleagues,

Biofilms are multicellular sessile microbial communities embedded in hydrated extracellular polymeric matrixes. This is common in microbial life in most environments, while those formed on food-processing surfaces are of considerable interest in the context of food hygiene. Biofilm cells express properties that are distinct from planktonic ones; one such property is their notorious resistance to antimicrobial agents. Thus, a special feature of biofilms is that, once they have been developed, these are hard to eradicate, even when typical sanitization procedures are regularly applied. A great deal of ongoing research has investigated how and why surface-attached microbial communities develop such resistances, and several mechanisms are to be acknowledged (e.g., heterogeneous metabolic activity, cell adaptive responses, diffusion limitations, genetic and functional diversification, and microbial interactions). This Special Issue aims to deliver deep insight into all these mechanisms, focusing on the role of biofilms in the development and dissemination of microbial resistance within the food industry.

Assist. Prof. Dr. Efstathios D. Giaouris
Assist. Prof. Dr. Manuel V. Simões
Prof. Dr. Florence Dubois-Brissonnet
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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. Foods is an international peer-reviewed open access semimonthly 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 2900 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

  • biofilms
  • microbial resistance
  • foods
  • disinfection
  • stress adaptation
  • antimicrobial agents

Published Papers (7 papers)

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Editorial

Jump to: Research, Review

5 pages, 208 KiB  
Editorial
The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry
by Efstathios Giaouris, Manuel Simões and Florence Dubois-Brissonnet
Foods 2020, 9(6), 816; https://doi.org/10.3390/foods9060816 - 21 Jun 2020
Cited by 14 | Viewed by 3204
Abstract
Biofilms are multicellular sessile microbial communities embedded in hydrated extracellular polymeric matrices. Their formation is common in microbial life in most environments, while those formed on food-processing surfaces are of considerable interest in the context of food hygiene. Biofilm cells express properties that [...] Read more.
Biofilms are multicellular sessile microbial communities embedded in hydrated extracellular polymeric matrices. Their formation is common in microbial life in most environments, while those formed on food-processing surfaces are of considerable interest in the context of food hygiene. Biofilm cells express properties that are distinct from planktonic ones, in particular, notorious resistance to antimicrobial agents. Thus, a special feature of biofilms is that, once they have been developed, they are hard to eradicate, even when careful sanitization procedures are regularly applied. A great deal of ongoing research has investigated how and why surface-attached microbial communities develop such resistance, and several mechanisms are to be acknowledged (e.g., heterogeneous metabolic activity, cell adaptive responses, diffusion limitations, genetic and functional diversification, and microbial interactions). The articles contained in this Special Issue deal with biofilms of some important food-related bacteria (including common pathogens such as Salmonella enterica, Listeria monocytogenes, and Staphylococcus aureus, as well as spoilage-causing spore-forming bacilli), providing novel insights on their resistance mechanisms and implications, together with novel methods (e.g., use of protective biofilms formed by beneficial bacteria, enzymes) that could be used to overcome such resistance and thus improve the safety of our food supply and protect public health. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)

Research

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14 pages, 2513 KiB  
Article
Robust Biofilm-Forming Bacillus Isolates from the Dairy Environment Demonstrate an Enhanced Resistance to Cleaning-in-Place Procedures
by Ievgeniia Ostrov, Tali Paz and Moshe Shemesh
Foods 2019, 8(4), 134; https://doi.org/10.3390/foods8040134 - 20 Apr 2019
Cited by 14 | Viewed by 5225
Abstract
One of the main strategies for maintaining the optimal hygiene level in dairy processing facilities is regular cleaning and disinfection, which is incorporated in the cleaning-in-place (CIP) regimes. However, a frail point of the CIP procedures is their variable efficiency in eliminating biofilm [...] Read more.
One of the main strategies for maintaining the optimal hygiene level in dairy processing facilities is regular cleaning and disinfection, which is incorporated in the cleaning-in-place (CIP) regimes. However, a frail point of the CIP procedures is their variable efficiency in eliminating biofilm bacteria. In the present study, we evaluated the susceptibility of strong biofilm-forming dairy Bacillus isolates to industrial cleaning procedures using two differently designed model systems. According to our results, the dairy-associated Bacillus isolates demonstrate a higher resistance to CIP procedures, compared to the non-dairy strain of B. subtilis. Notably, the tested dairy isolates are highly persistent to different parameters of the CIP operations, including the turbulent flow of liquid (up to 1 log), as well as the cleaning and disinfecting effects of commercial detergents (up to 2.3 log). Moreover, our observations indicate an enhanced resistance of poly-γ-glutamic acid (PGA)-overproducing B. subtilis, which produces high amounts of proteinaceous extracellular matrix, to the CIP procedures (about 0.7 log, compared to the wild-type non-dairy strain of B. subtilis). We therefore suggest that the enhanced resistance to the CIP procedures by the dairy Bacillus isolates can be attributed to robust biofilm formation. In addition, this study underlines the importance of evaluating the efficiency of commercial cleaning agents in relation to strong biofilm-forming bacteria, which are relevant to industrial conditions. Consequently, we believe that the findings of this study can facilitate the assessment and refining of the industrial CIP procedures. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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8 pages, 1646 KiB  
Article
Biofilm Challenge: Lactic Acid Bacteria Isolated from Bovine Udders versus Staphylococci
by Jonathan K. Wallis, Volker Krömker and Jan-Hendrik Paduch
Foods 2019, 8(2), 79; https://doi.org/10.3390/foods8020079 - 20 Feb 2019
Cited by 23 | Viewed by 5208
Abstract
Mastitis poses a considerable threat to productivity and to animal welfare on modern dairy farms. However, the common way of antibiotic treatment does not always lead to a cure. Unsuccessful cures can, among other reasons, occur due to biofilm formation of the causative [...] Read more.
Mastitis poses a considerable threat to productivity and to animal welfare on modern dairy farms. However, the common way of antibiotic treatment does not always lead to a cure. Unsuccessful cures can, among other reasons, occur due to biofilm formation of the causative agent. This has attracted interest from researchers to introduce promising alternative therapeutic approaches, such as the use of beneficial lactic acid bacteria (LAB). In fact, using LAB for treating mastitis probably requires the formation of a beneficial biofilm by the probiotic bacteria. The present study investigated the ability of five LAB strains, selected on the basis of results from previous studies, to remove and to replace pathogenic biofilms in vitro. For this purpose, Staphylococcus (S.) aureus ATCC 12,600 and two strains—S. xylosus (35/07) and S. epidermidis (575/08)—belonging to the group of coagulase negative staphylococci (CNS) were allowed to form biofilms in a 96-well plate. Subsequently, the LAB were added to the well. The biofilm challenge was evaluated by scraping off and suspending the biofilm cells, followed by a plate count of serial dilutions using selective media. All the LAB strains successfully removed the staphylococcal biofilms. However, only Lactobacillus (L.) rhamnosus ATCC 7469 and L. plantarum 2/37 formed biofilms of their own to replace the pathogenic ones. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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12 pages, 1028 KiB  
Article
Antibiofilm Effect of DNase against Single and Mixed Species Biofilm
by Komal Sharma and Ankita Pagedar Singh
Foods 2018, 7(3), 42; https://doi.org/10.3390/foods7030042 - 19 Mar 2018
Cited by 51 | Viewed by 7850
Abstract
Biofilms are aggregates of microorganisms that coexist in socially coordinated micro-niche in a self-produced polymeric matrix on pre-conditioned surfaces. The biofilm matrix reduces the efficacy of antibiofilm strategies. DNase degrades the extracellular DNA (e-DNA) present in the matrix, rendering the matrix weak and [...] Read more.
Biofilms are aggregates of microorganisms that coexist in socially coordinated micro-niche in a self-produced polymeric matrix on pre-conditioned surfaces. The biofilm matrix reduces the efficacy of antibiofilm strategies. DNase degrades the extracellular DNA (e-DNA) present in the matrix, rendering the matrix weak and susceptible to antimicrobials. In the current study, the effect of DNase I was evaluated during biofilm formation (pre-treatment), on preformed biofilms (post-treatment) and both (dual treatment). The DNase I pre-treatment was optimized for P. aeruginosa PAO1 (model biofilm organism) at 10 µg/mL and post-treatment at 10 µg/mL with 15 min of contact duration. Inclusion of Mg2+ alongside DNase I post-treatment resulted in 90% reduction in biofilm within only 5 min of contact time (irrespective of age of biofilm). On extension of these findings, DNase I was found to be less effective against mixed species biofilm than individual biofilms. DNase I can be used as potent antibiofilm agent and with further optimization can be effectively used for biofilm prevention and reduction in situ. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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591 KiB  
Article
Effect of Food Residues in Biofilm Formation on Stainless Steel and Polystyrene Surfaces by Salmonella enterica Strains Isolated from Poultry Houses
by Alba María Paz-Méndez, Alexandre Lamas, Beatriz Vázquez, José Manuel Miranda, Alberto Cepeda and Carlos Manuel Franco
Foods 2017, 6(12), 106; https://doi.org/10.3390/foods6120106 - 29 Nov 2017
Cited by 25 | Viewed by 6664
Abstract
Salmonella spp. is a major food-borne pathogen around the world. The ability of Salmonella to produce biofilm is one of the main obstacles in reducing the prevalence of these bacteria in the food chain. Most of Salmonella biofilm studies found in the literature [...] Read more.
Salmonella spp. is a major food-borne pathogen around the world. The ability of Salmonella to produce biofilm is one of the main obstacles in reducing the prevalence of these bacteria in the food chain. Most of Salmonella biofilm studies found in the literature used laboratory growth media. However, in the food chain, food residues are the principal source of nutrients of Salmonella. In this study, the biofilm formation, morphotype, and motility of 13 Salmonella strains belonging to three different subspecies and isolated from poultry houses was evaluated. To simulate food chain conditions, four different growth media (Tryptic Soy Broth at 1/20 dilution, milk at 1/20 dilution, tomato juice, and chicken meat juice), two different surfaces (stainless steel and polystyrene) and two temperatures (6 °C and 22 °C) were used to evaluate the biofilm formation. The morphotype, motility, and biofilm formation of Salmonella was temperature-dependent. Biofilm formation was significantly higher with 1/20 Tryptic Soy Broth in all the surfaces and temperatures tested, in comparison with the other growth media. The laboratory growth medium 1/20 Tryptic Soy Broth enhanced biofilm formation in Salmonella. This could explain the great differences in biofilm formation found between this growth medium and food residues. However, Salmonella strains were able to produce biofilm on the presence of food residues in all the conditions tested. Therefore, the Salmonella strain can use food residues to produce biofilm on common surfaces of the food chain. More studies combining more strains and food residues are necessary to fully understand the mechanism used by Salmonella to produce biofilm on the presence of these sources of nutrients. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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Review

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16 pages, 630 KiB  
Review
Understanding Antimicrobial Resistance (AMR) Profiles of Salmonella Biofilm and Planktonic Bacteria Challenged with Disinfectants Commonly Used During Poultry Processing
by Myrna Cadena, Todd Kelman, Maria L. Marco and Maurice Pitesky
Foods 2019, 8(7), 275; https://doi.org/10.3390/foods8070275 - 22 Jul 2019
Cited by 51 | Viewed by 8744
Abstract
Foodborne pathogens such as Salmonella that survive cleaning and disinfection during poultry processing are a public health concern because pathogens that survive disinfectants have greater potential to exhibit resistance to antibiotics and disinfectants after their initial disinfectant challenge. While the mechanisms conferring antimicrobial [...] Read more.
Foodborne pathogens such as Salmonella that survive cleaning and disinfection during poultry processing are a public health concern because pathogens that survive disinfectants have greater potential to exhibit resistance to antibiotics and disinfectants after their initial disinfectant challenge. While the mechanisms conferring antimicrobial resistance (AMR) after exposure to disinfectants is complex, understanding the effects of disinfectants on Salmonella in both their planktonic and biofilm states is becoming increasingly important, as AMR and disinfectant tolerant bacteria are becoming more prevalent in the food chain. This review examines the modes of action of various types of disinfectants commonly used during poultry processing (quaternary ammonium, organic acids, chlorine, alkaline detergents) and the mechanisms that may confer tolerance to disinfectants and cross-protection to antibiotics. The goal of this review article is to characterize the AMR profiles of Salmonella in both their planktonic and biofilm state that have been challenged with hexadecylpyridinium chloride (HDP), peracetic acid (PAA), sodium hypochlorite (SHY) and trisodium phosphate (TSP) in order to understand the risk of these disinfectants inducing AMR in surviving bacteria that may enter the food chain. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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19 pages, 336 KiB  
Review
Current Knowledge on Listeria monocytogenes Biofilms in Food-Related Environments: Incidence, Resistance to Biocides, Ecology and Biocontrol
by Pedro Rodríguez-López, Juan José Rodríguez-Herrera, Daniel Vázquez-Sánchez and Marta López Cabo
Foods 2018, 7(6), 85; https://doi.org/10.3390/foods7060085 - 05 Jun 2018
Cited by 94 | Viewed by 8292
Abstract
Although many efforts have been made to control Listeria monocytogenes in the food industry, growing pervasiveness amongst the population over the last decades has made this bacterium considered to be one of the most hazardous foodborne pathogens. Its outstanding biocide tolerance capacity and [...] Read more.
Although many efforts have been made to control Listeria monocytogenes in the food industry, growing pervasiveness amongst the population over the last decades has made this bacterium considered to be one of the most hazardous foodborne pathogens. Its outstanding biocide tolerance capacity and ability to promiscuously associate with other bacterial species forming multispecies communities have permitted this microorganism to survive and persist within the industrial environment. This review is designed to give the reader an overall picture of the current state-of-the-art in L. monocytogenes sessile communities in terms of food safety and legislation, ecological aspects and biocontrol strategies. Full article
(This article belongs to the Special Issue The Role of Biofilms in the Development and Dissemination of Microbial Resistance within the Food Industry)
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