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The Challenge of Biofilms in the Food Industry: Formation, Prevention...
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The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control

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

Deadline for manuscript submissions: closed (20 February 2023) | Viewed by 25443

Special Issue Editors

Dr. Pilar Teixeira

E-Mail Website
Guest Editor
LIBRO—Laboratório de Investigação em Biofilmes Rosário Oliveira, Centre of Biological Engineering, University of Minho, 4710-057 Braga, Portugal
Interests: cell adhesion; cell viability; biofilms; antimicrobial strategies; foodborne pathogens; food safety
Dr. Carina Almeida

E-Mail Website
Guest Editor
INIAV, IP—National Institute for Agrarian and Veterinary Research, Rua dos Lagidos, Lugar da Madalena, 4485-655 Vairão, Vila do Conde, Portugal
Interests: clinical pathogens; foodborne pathogens; antibiotic resistance; surveillance; food and clinical-related biofilms
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Biofilms cause significant financial losses in the food industry, since the presence of biofilms along processing surfaces can result in corrosion and biofouling. This may imply the need to replace some pieces of equipment and higher energy consumption. Moreover, the alteration of organoleptic properties due to the secretion of lipases or proteases by some bacteria makes food unfit for consumption, which also entails economic losses. However, the most serious problem posed by biofilms is related with food poisoning, as some biofilm-forming species in food environments are human foodborne pathogens. According to food safety research, approximately 60 percent of foodborne illness outbreaks are caused by biofilms. This arises from the capacity of bacteria to easily adhere to food processing surfaces and to form biofilms, which are more difficult to remove from the surfaces by mechanical washing and cleaning and are also more resilient to disinfection procedures. In fact, the increased inherent resistance of biofilm bacteria to biocides is the major factor affecting plant sanitation and product safety.

Thus, it is urgent to deepen the knowledge regarding biofilms considering all perspectives relevant to the food industry, including the formation of biofilms and their structure, disinfection resistance and new strategies for targeting them. Also of great importance is the role of biofilms in cross-contamination at the retail level and its relevant in the overall picture of food contamination/outbreaks.

With this Special Issue, we aim to gather a collection of articles that boost our knowledge on food-associated biofilms, their real impact on food safety and quality, and innovative strategies that can help industry and retailers in managing this problem. We hope that helpful information can be gathered and used by relevant stockholders to increase food security/quality and, ultimately, to protect public health. Original research articles and reviews are welcome.

Dr. Pilar Teixeira
Dr. Carina Almeida
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

  • biofilm formation
  • biofilm structure
  • food industry
  • food spoilage
  • foodborne pathogens
  • new antibiofilm strategies
  • food safety

Published Papers (9 papers)

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Research

19 pages, 4332 KiB  
Article
Characterization of the Biofilms Formed by Histamine-Producing Lentilactobacillus parabuchneri Strains in the Dairy Environment
by Agustina Sarquis, Diellza Bajrami, Boris Mizaikoff, Victor Ladero, Miguel A. Alvarez and Maria Fernandez
Foods 2023, 12(7), 1503; https://0-doi-org.brum.beds.ac.uk/10.3390/foods12071503 - 03 Apr 2023
Cited by 4 | Viewed by 7860
Abstract
Lentilactobacillus parabuchneri, a lactic acid bacterium, is largely responsible for the production and accumulation of histamine, a toxic biogenic amine, in cheese. L. parabuchneri strains can form biofilms on the surface of industry equipment. Since they are resistant to cleaning and disinfection, [...] Read more.
Lentilactobacillus parabuchneri, a lactic acid bacterium, is largely responsible for the production and accumulation of histamine, a toxic biogenic amine, in cheese. L. parabuchneri strains can form biofilms on the surface of industry equipment. Since they are resistant to cleaning and disinfection, they may act as reservoirs of histamine-producing contaminants in cheese. The aim of this study was to investigate the biofilm-producing capacity of L. parabuchneri strains. Using the crystal violet technique, the strains were first categorized as weak, moderate or strong biofilm producers. Analysis of their biofilm matrices revealed them to be mainly composed of proteins. Two strains of each category were then selected to analyze the influence on the biofilm-forming capacity of temperature, pH, carbon source, NaCl concentration and surface material (i.e., focusing on those used in the dairy industry). In general, low temperature (8 °C), high NaCl concentrations (2–3% w/v) and neutral pH (pH 6) prevented biofilm formation. All strains were found to adhere easily to beech wood. These findings increase knowledge of the biofilm-forming capacity of histamine-producing L. parabuchneri strains and how their formation may be prevented for improving food safety. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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16 pages, 1155 KiB  
Article
Activity of Binary Combinations of Natural Phenolics and Synthetic Food Preservatives against Food Spoilage Yeasts
by Bernard Gitura Kimani, Miklós Takó, Csilla Veres, Judit Krisch, Tamás Papp, Erika Beáta Kerekes and Csaba Vágvölgyi
Foods 2023, 12(6), 1338; https://0-doi-org.brum.beds.ac.uk/10.3390/foods12061338 - 22 Mar 2023
Cited by 3 | Viewed by 1629
Abstract
Natural compounds are a suitable alternative to synthetic food preservatives due to their natural origin and health-promoting properties. In the current study, phenolic–phenolic and phenolic–synthetic combinations were tested for their antibiofilm formation, anti-planktonic growth, and anti-adhesion properties against Debaryomyces hansenii, Wickerhamomyces anomalus [...] Read more.
Natural compounds are a suitable alternative to synthetic food preservatives due to their natural origin and health-promoting properties. In the current study, phenolic–phenolic and phenolic–synthetic combinations were tested for their antibiofilm formation, anti-planktonic growth, and anti-adhesion properties against Debaryomyces hansenii, Wickerhamomyces anomalus (formerly Pichia anomala), Schizosaccharomyces pombe, and Saccharomyces cerevisiae. The phenolics were vanillin and cinnamic acid, while the synthetic preservatives were sodium benzoate, potassium sorbate, and sodium diacetate. The vanillin–cinnamic acid combination had synergistic effect in all the tested yeasts for the biofilm inhibition with a fractional inhibitory concentration index (FICI) of ≤0.19 for W. anomalus, 0.25 for S. pombe, 0.31 for S. cerevisiae, and 0.5 for D. hansenii. Most of the phenolic–synthetic combinations had indifferent interaction regarding biofilm formation. The vanillin–cinnamic acid combination also had higher activity against spoilage yeasts adhesion on the abiotic surface and planktonic growth compared to the phenolic–synthetic combinations. For the phenolic–synthetic anti-planktonic activity, synergistic interaction was present in all the vanillin–synthetic combinations in S. pombe, vanillin–sodium benzoate and vanillin–potassium sorbate in S. cerevisiae, vanillin–sodium benzoate in W. anomalus, and cinnamic acid–sodium diacetate in S. pombe. These results suggest a novel antimicrobial strategy that may broaden the antimicrobial spectrum and reduce compound toxicity against food spoilage yeasts. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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17 pages, 4611 KiB  
Article
Inhibition of Cronobacter sakazakii by Litsea cubeba Essential Oil and the Antibacterial Mechanism
by Haoran Wang, Yulu Li, Zhuo Li, Run Ma, Xiangyang Bai, Xiangjun Zhan, Kunyao Luo, Ruiying Su, Xuejiao Li, Xiaodong Xia and Chao Shi
Foods 2022, 11(23), 3900; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11233900 - 02 Dec 2022
Cited by 6 | Viewed by 1963
Abstract
Litsea cubeba essential oil (LC-EO) has anti-insecticidal, antioxidant, and anticancer proper-ties; however, its antimicrobial activity toward Cronobacter sakazakii has not yet been researched extensively. The objective of this study was to investigate the antimicrobial and antibiofilm effects of LC-EO toward C. sakazakii, [...] Read more.
Litsea cubeba essential oil (LC-EO) has anti-insecticidal, antioxidant, and anticancer proper-ties; however, its antimicrobial activity toward Cronobacter sakazakii has not yet been researched extensively. The objective of this study was to investigate the antimicrobial and antibiofilm effects of LC-EO toward C. sakazakii, along with the underlying mechanisms. The minimum inhibitory concentrations of LC-EO toward eight different C. sakazakii strains ranged from 1.5 to 4.0 μL/mL, and LC-EO exposure showed a longer lag phase and lower specific growth compared to untreated bacteria. LC-EO increased reactive oxygen species production, decreased the integrity of the cell membrane, caused cell membrane depolarization, and decreased the ATP concentration in the cell, showing that LC-EO caused cellular damage associated with membrane permeability. LC-EO induced morphological changes in the cells. LC-EO inhibited C. sakazakii in reconstituted infant milk formula at 50 °C, and showed effective inactivation of C. sakazakii biofilms on stainless steel surfaces. Confocal laser scanning and attenuated total reflection–Fourier-transform infrared spectrometry indicated that the biofilms were disrupted by LC-EO. These findings suggest a potential for applying LC-EO in the prevention and control of C. sakazakii in the dairy industry as a natural antimicrobial and antibiofilm agent. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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14 pages, 3379 KiB  
Article
Propionate and Butyrate Inhibit Biofilm Formation of Salmonella Typhimurium Grown in Laboratory Media and Food Models
by Jiaxiu Liu, Wenxiu Zhu, Ningbo Qin, Xiaomeng Ren and Xiaodong Xia
Foods 2022, 11(21), 3493; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11213493 - 03 Nov 2022
Cited by 12 | Viewed by 1867
Abstract
Salmonella is among the most frequently isolated foodborne pathogens, and biofilm formed by Salmonella poses a potential threat to food safety. Short-chain fatty acids (SCFAs), especially propionate and butyrate, have been demonstrated to exhibit a beneficial effect on promoting intestinal health and regulating [...] Read more.
Salmonella is among the most frequently isolated foodborne pathogens, and biofilm formed by Salmonella poses a potential threat to food safety. Short-chain fatty acids (SCFAs), especially propionate and butyrate, have been demonstrated to exhibit a beneficial effect on promoting intestinal health and regulating the host immune system, but their anti-biofilm property has not been well studied. This study aims to investigate the effects of propionate or butyrate on the biofilm formation and certain virulence traits of Salmonella. We investigated the effect of propionate or butyrate on the biofilm formation of Salmonella enterica serovar Typhimurium (S. Typhimurium) SL1344 grown in LB broth or food models (milk or chicken juice) by crystal violet staining methods. Biofilm formation was significantly reduced in LB broth and food models and the reduction was visualized using a scanning electron microscope (SEM). Biofilm metabolic activity was attenuated in the presence of propionate or butyrate. Meanwhile, both SCFAs decreased AI-2 quorum sensing based on reporter strain assay. Butyrate, not propionate, could effectively reduce bacterial motility. Bacterial adhesion to and invasion of Caco-2 cells were also significantly inhibited in the presence of both SCFAs. Finally, two SCFAs downregulated virulence genes related to biofilm formation and invasion through real-time polymerase chain reaction (RT-PCR). These findings demonstrate the potential application of SCFAs in the mitigation of Salmonella biofilm in food systems, but future research mimicking food environments encountered during the food chain is necessitated. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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11 pages, 1019 KiB  
Communication
Bacterial Attachment and Biofilm Formation on Antimicrobial Sealants and Stainless Steel Surfaces
by Luminita Ciolacu, Elena Zand, Carmen Negrau and Henry Jaeger
Foods 2022, 11(19), 3096; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11193096 - 05 Oct 2022
Cited by 5 | Viewed by 1900
Abstract
Biofilms are highly resistant to external forces, especially chemicals. Hence, alternative control strategies, like antimicrobial substances, are forced. Antimicrobial surfaces can inhibit and reduce microbial adhesion to surfaces, preventing biofilm formation. Thus, this research aimed to investigate the bacterial attachment and biofilm formation [...] Read more.
Biofilms are highly resistant to external forces, especially chemicals. Hence, alternative control strategies, like antimicrobial substances, are forced. Antimicrobial surfaces can inhibit and reduce microbial adhesion to surfaces, preventing biofilm formation. Thus, this research aimed to investigate the bacterial attachment and biofilm formation on different sealants and stainless steel (SS) surfaces with or without antimicrobials on two Gram-positive biofilm forming bacterial strains. Antimicrobial surfaces were either incorporated or coated with anti-microbial, -fungal or/and bactericidal agents. Attachment (after 3 h) and early-stage biofilm formation (after 48 h) of Staphylococcus capitis (S. capitis) and Microbacterium lacticum (M. lacticum) onto different surfaces were assessed using the plate count method. In general, bacterial adhesion on sealants was lower compared to adhesion on SS, for surfaces with and without antimicrobials. Antimicrobial coatings on SS surfaces played a role in reducing early-stage biofilm formation for S. capitis, however, no effects were observed for M. lacticum. S. capitis adhesion and biofilm formation were reduced by 8% and 25%, respectively, on SS coated with an antimicrobial substance (SS_4_M), compared to the same surface without the antimicrobial coating (SS_4_control). Incorporation of both antifungicidal and bactericidal agents (S_5_FB) significantly reduced (p ≤ 0.05) early-stage biofilm formation of M. lacticum, compared to the other sealants incoportating either solely antifungal agents (S_2_F) or no active compound (S_control). Furthermore, the thickness of the coating layer correlated weakly with the antimicrobial effect. Hence, equipment manufacturers and food producers should carefully select antimicrobial surfaces as their effects on bacterial adhesion and early-stage biofilm formation depend on the active agent and bacterial species. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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13 pages, 1746 KiB  
Article
Bacteriocin Production by Escherichia coli during Biofilm Development
by Hanna Fokt, Sara Cleto, Hugo Oliveira, Daniela Araújo, Joana Castro, Nuno Cerca, Maria João Vieira and Carina Almeida
Foods 2022, 11(17), 2652; https://doi.org/10.3390/foods11172652 - 01 Sep 2022
Cited by 2 | Viewed by 1879
Abstract
Escherichia coli is a highly versatile bacterium ranging from commensal to intestinal pathogen, and is an important foodborne pathogen. E. coli species are able to prosper in multispecies biofilms and secrete bacteriocins that are only toxic to species/strains closely related to the producer [...] Read more.
Escherichia coli is a highly versatile bacterium ranging from commensal to intestinal pathogen, and is an important foodborne pathogen. E. coli species are able to prosper in multispecies biofilms and secrete bacteriocins that are only toxic to species/strains closely related to the producer strain. In this study, 20 distinct E. coli strains were characterized for several properties that confer competitive advantages against closer microorganisms by assessing the biofilm-forming capacity, the production of antimicrobial molecules, and the production of siderophores. Furthermore, primer sets for E. coli bacteriocins–colicins were designed and genes were amplified, allowing us to observe that colicins were widely distributed among the pathogenic E. coli strains. Their production in the planktonic phase or single-species biofilms was uncommon. Only two E. coli strains out of nine biofilm-forming were able to inhibit the growth of other E. coli strains. There is evidence of larger amounts of colicin being produced in the late stages of E. coli biofilm growth. The decrease in bacterial biomass after 12 h of incubation indicates active type I colicin production, whose release normally requires E. coli cell lysis. Almost all E. coli strains were siderophore-producing, which may be related to the resistance to colicin as these two molecules may use the same transporter system. Moreover, E. coli CECT 504 was able to coexist with Salmonella enterica in dual-species biofilms, but Shigella dysenteriae was selectively excluded, correlating with high expression levels of colicin (E, B, and M) genes observed by real-time PCR. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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16 pages, 2733 KiB  
Article
Antibacterial Effect of Eugenol on Shigella flexneri and Its Mechanism
by Xiangyang Bai, Xuejiao Li, Xue Liu, Zeyu Xing, Ruiying Su, Yutang Wang, Xiaodong Xia and Chao Shi
Foods 2022, 11(17), 2565; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11172565 - 25 Aug 2022
Cited by 13 | Viewed by 2313
Abstract
Shigella flexneri (Sh. flexneri), which can be found in food and the environment, is a widespread food-borne pathogen that causes human diarrhea termed “shigellosis”. In this study, eugenol, a natural active substance, was investigated for its antibacterial activity against Sh. flexneri [...] Read more.
Shigella flexneri (Sh. flexneri), which can be found in food and the environment, is a widespread food-borne pathogen that causes human diarrhea termed “shigellosis”. In this study, eugenol, a natural active substance, was investigated for its antibacterial activity against Sh. flexneri. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of eugenol against Sh. flexneri ATCC 12022 was 0.5 and 0.8 mg/mL. The growth curves and inhibitory effect in LB broth, PBS, vegetable juice, and minced pork showed that eugenol had a good activity against Sh. flexneri. Research findings indicated the superoxide dismutase activity of Sh. flexneri was inhibited after eugenol treatment, resulting in concentrations of intracellular reactive oxygen species and an increase in malondialdehyde. The flow cytometry analysis and field emission scanning electron microscopy results revealed obvious damage to cell membrane integrity and changes in the morphology of Sh. flexneri. In addition, the intracellular ATP concentration leaked from 0.5 μM to below 0.05 μM and the membrane potential showed a concentration-dependent depolarization after eugenol treatment. In summary, eugenol exerted strong antibacterial activity and has the potential to control Sh. flexneri in the food industry. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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19 pages, 4342 KiB  
Article
The Antimicrobial and Antibiofilm Activity of Oregano Essential Oil against Enterococcus faecalis and Its Application in Chicken Breast
by Xiangjun Zhan, Yingzhu Tan, Yingmei Lv, Jianing Fang, Yuanjian Zhou, Xing Gao, Huimin Zhu and Chao Shi
Foods 2022, 11(15), 2296; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11152296 - 01 Aug 2022
Cited by 6 | Viewed by 2567
Abstract
Oregano essential oil (OEO) possesses anti-inflammatory, antioxidant, and cancer-suppressive properties. Enterococcus faecalis is a foodborne opportunistic pathogen that can be found in nature and the food processing industry. The goal of this investigation was to explore the antimicrobial action and mechanism of OEO [...] Read more.
Oregano essential oil (OEO) possesses anti-inflammatory, antioxidant, and cancer-suppressive properties. Enterococcus faecalis is a foodborne opportunistic pathogen that can be found in nature and the food processing industry. The goal of this investigation was to explore the antimicrobial action and mechanism of OEO against E. faecalis, inactivation action of OEO on E. faecalis in mature biofilms, and its application in chicken breast. The minimum inhibitory concentration (MIC) of OEO against E. faecalis strains (ATCC 29212 and nine isolates) ranged from 0.25 to 0.50 μL/mL. OEO therapy reduced intracellular adenosine triphosphate (ATP) levels, caused cell membrane hyperpolarization, increased the intracellular reactive oxygen species (ROS), and elevated extracellular malondialdehyde (MDA) concentrations. Furthermore, OEO treatment diminished cell membrane integrity and caused morphological alterations in the cells. In biofilms on stainless-steel, OEO showed effective inactivation activity against E. faecalis. OEO reduced the number of viable cells, cell viability and exopolysaccharides in the biofilm, as well as destroying its structure. Application of OEO on chicken breast results in a considerable reduction in E. faecalis counts and pH values, in comparison to control samples. These findings suggest that OEO could be utilized as a natural antibacterial preservative and could effectively control E. faecalis in food manufacturing. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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21 pages, 4526 KiB  
Article
Inactivation of Polymicrobial Biofilms of Foodborne Pathogens Using Epsilon Poly-L-Lysin Conjugated Chitosan Nanoparticles
by Xingjian Bai, Luping Xu, Atul Kumar Singh, Xiaoling Qiu, Mai Liu, Ahmed Abuzeid, Talaat El-Khateib and Arun K. Bhunia
Foods 2022, 11(4), 569; https://0-doi-org.brum.beds.ac.uk/10.3390/foods11040569 - 16 Feb 2022
Cited by 6 | Viewed by 2115
Abstract
A mixed culture (polymicrobial) biofilm provides a favorable environment for pathogens to persist in the food processing environment and to contaminate food products. Inactivation and eradication of such biofilms from food processing environments are achieved by using harsh disinfectants, but their toxicity and [...] Read more.
A mixed culture (polymicrobial) biofilm provides a favorable environment for pathogens to persist in the food processing environment and to contaminate food products. Inactivation and eradication of such biofilms from food processing environments are achieved by using harsh disinfectants, but their toxicity and environmentally hostile characteristics are unsustainable. This study aims to use food-grade natural nanoparticulated antimicrobials to control mixed-culture biofilms. Chitosan, a natural broad-spectrum antimicrobial biopolymer (polysaccharide) from crustaceans, was derivatized to produce chitosan nanoparticles (ChNP) as a carrier for another broad-spectrum antimicrobial agent, ε-poly-L-lysine (PL), to synthesize ChNP-PL conjugate. The antimicrobial activity of ChNP and ChNP-PL was tested against mixed-culture biofilms. ChNP-PL (~100 nm) exhibited a synergistic antimicrobial and anti-biofilm effect against mono or mixed-culture biofilms of five foodborne pathogens, including Listeria monocytogenes, Staphylococcus aureus, Salmonella enterica serovar Enteritidis, Escherichia coli O157:H7, and Pseudomonas aeruginosa. ChNP-PL treatment prevented biofilm formation by mono or mixed cultures of L. monocytogenes, P. aeruginosa, and E. coli O157:H7, and bacterial counts were either below the detection limit or caused 3.5–5 log reduction. ChNP-PL also inactivated preformed biofilms. In monoculture biofilm, ChNP-PL treatment reduced L. monocytogenes counts by 4.5 logs, S. Enteritidis by 2 logs, E. coli by 2 logs, and S. aureus by 0.5 logs, while ChNP-PL had no inhibitory effect on P. aeruginosa. In vitro mammalian cell-based cytotoxicity analysis confirmed ChNP-PL to have no deleterious effect on intestinal HCT-8 cell line. In conclusion, our results show ChNP-PL has strong potential to prevent the formation or inactivation of preformed polymicrobial biofilms of foodborne pathogens. Full article
(This article belongs to the Special Issue The Challenge of Biofilms in the Food Industry: Formation, Prevention and Control)
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