The Impact and Applications of Phages in the Food Industry and Agriculture

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Bacterial Viruses".

Deadline for manuscript submissions: closed (30 April 2019) | Viewed by 74693

Special Issue Editors

University College Cork, APC Microbiome Ireland, Cork, Ireland
Interests: gut microbiota; comparative and functional genomics; molecular microbiology; bacteriophages; human gut commensal bacteria
Special Issues, Collections and Topics in MDPI journals
APC Microbiome Ireland & School of Microbiology, University College Cork, Cork, Ireland

Special Issue Information

Dear Colleagues,

The food industry (and its component agri-food sector) is a multi-billion dollar global industry, reliant on the production of foods with desirable organoleptic and physical properties. Dairy fermentations are consistently challenged by the presence of bacteriophages (phages), which may infect the lactic acid bacterial starter or adjunct cultures. Such infections may lead to slow or even failed fermentations with significant economic consequences. Therefore, phages infecting the lactic acid bacteria (LAB) have been the subject of intense research scrutiny for a number of decades with a view to developing detection and classification tools, anti-phage strategies while simultaneously improving starter culture selection and rotation schemes. In contrast to the undesirable presence of phages in dairy fermentations, they are viewed more favourably in the context of food safety where they may be applied to control or eliminate bacterial contaminants. For example, phages that target common food contaminants and pathogens including Campylobacter, Salmonella, Escherichia coli, Listeria and Staphylococcus spp. have received significant research attention in recent years in an effort to improve the safety and/or quality of a variety of foods. Phage-based solutions to food spoilage and contamination may potentially be applied at various stages of food/beverage production, processing and packaging. This has implications for meat, dairy and (alcoholic) beverage production systems, among others and may include intact phages/phage cocktails or phage-derived products, such as phage-encoded lysins or their engineered derivatives. Furthermore, reporter phage systems have been established for the rapid identification of food spoilage organisms and pathogens that represent the next generation of diagnostic tools for the food industry to limit the dissemination of contaminated food products to the public.

In this Special Issue, we invite authors to submit unpublished original contributions and critical reviews covering topics relating to the research of phages that either negatively impact food fermentations or that may be beneficially applied to improve the microbial safety and/or quality of food or beverages. This may include themes such as phage ecology in food fermentations, phage-host interactions and the application of phages or their derived components as biocontrol or biosensors in the food industry.


Dr. Jennifer Mahony
Dr. Douwe Van Sinderen
Dr. Eoghan Casey
Guest Editors

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Keywords

  • phage ecology
  • food fermentations
  • phage biosensors
  • phage lysine and food safety

Published Papers (13 papers)

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Editorial

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3 pages, 171 KiB  
Editorial
The Impact and Applications of Phages in the Food Industry and Agriculture
by Jennifer Mahony, Eoghan Casey and Douwe van Sinderen
Viruses 2020, 12(2), 210; https://0-doi-org.brum.beds.ac.uk/10.3390/v12020210 - 13 Feb 2020
Cited by 4 | Viewed by 2616
Abstract
Food security is currently a global socio-political pressure point that is exacerbated by the ever-increasing world population [...] Full article

Research

Jump to: Editorial, Review

12 pages, 616 KiB  
Article
The Effect of a Commercially Available Bacteriophage and Bacteriocin on Listeria monocytogenes in Coleslaw
by Rhea Lewis, Andrei Sorin Bolocan, Lorraine A. Draper, R. Paul Ross and Colin Hill
Viruses 2019, 11(11), 977; https://0-doi-org.brum.beds.ac.uk/10.3390/v11110977 - 23 Oct 2019
Cited by 18 | Viewed by 4679
Abstract
Changing consumer attitudes show an increased interest in non-chemical antimicrobials in food preservation and safety. This greater interest of consumers in more ‘natural’ or ‘clean-label’ food interventions is complicated by concurrent demands for minimally processed, ready-to-eat (RTE) foods with long shelf lives. Two [...] Read more.
Changing consumer attitudes show an increased interest in non-chemical antimicrobials in food preservation and safety. This greater interest of consumers in more ‘natural’ or ‘clean-label’ food interventions is complicated by concurrent demands for minimally processed, ready-to-eat (RTE) foods with long shelf lives. Two viable interventions are bacteriophage (phage) and bacteriocins, a number of which have already been approved for use in food safety. Listeriosis is a serious foodborne infection which affects at-risk members of the population. Listeriosis incidence has increased between 2008 and 2015 and has a case fatality rate of up to 20% with antibiotic intervention. Here, we tested an intervention to attempt to control a pathogenic Listeria monocytogenes strain in a food model using two of these alternative antimicrobials. Phage P100 on its own had a significant effect on L. monocytogenes ScottA numbers in coleslaw over a 10-day period at 4 °C (p ≤ 0.001). A combination of P100 and Nisaplin® (a commercial formulation of the lantibiotic bacteriocin, nisin) had a significant effect on the pathogen (p ≤ 0.001). P100 and Nisaplin® in combination were more effective than Nisaplin® alone, but not P100 alone. Full article
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14 pages, 1791 KiB  
Article
Inhibition of L. monocytogenes Biofilm Formation by the Amidase Domain of the Phage vB_LmoS_293 Endolysin
by Vincenzo Pennone, Marta Sanz-Gaitero, Paula O’Connor, Aidan Coffey, Kieran Jordan, Mark J. van Raaij and Olivia McAuliffe
Viruses 2019, 11(8), 722; https://0-doi-org.brum.beds.ac.uk/10.3390/v11080722 - 06 Aug 2019
Cited by 25 | Viewed by 4863
Abstract
Listeria monocytogenes is a ubiquitous Gram-positive bacterium that is a major concern for food business operators because of its pathogenicity and ability to form biofilms in food production environments. Bacteriophages (phages) have been evaluated as biocontrol agents for L. monocytogenes in a number [...] Read more.
Listeria monocytogenes is a ubiquitous Gram-positive bacterium that is a major concern for food business operators because of its pathogenicity and ability to form biofilms in food production environments. Bacteriophages (phages) have been evaluated as biocontrol agents for L. monocytogenes in a number of studies and, indeed, certain phages have been approved for use as anti-listerial agents in food processing environments (ListShield and PhageGuard Listex). Endolysins are proteins produced by phages in the host cell. They cleave the peptidoglycan cell wall, thus allowing release of progeny phage into the environment. In this study, the amidase domain of the phage vB_LmoS_293 endolysin (293-amidase) was cloned and expressed in Escherichia. coli (E. coli). Muralytic activity at different concentrations, pH and temperature values, lytic spectrum and activity against biofilms was determined for the purified 293-amidase protein. The results showed activity on autoclaved cells at three different temperatures (20 °C, 37 °C and 50 °C), with a wider specificity (L. monocytogenes 473 and 3099, a serotype 4b and serogroup 1/2b-3b-7, respectively) compared to the phage itself, which targets only L. monocytogenes serotypes 4b and 4e. The protein also inhibits biofilm formation on abiotic surfaces. These results show the potential of using recombinant antimicrobial proteins against pathogens in the food production environment. Full article
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12 pages, 2155 KiB  
Article
Application of the Phage Lysin Ply5218 in the Treatment of Streptococcus suis Infection in Piglets
by Zhaofei Wang, Jingjiao Ma, Jian Wang, Denghui Yang, Licheng Kong, Qiang Fu, Yuqiang Cheng, Hengan Wang, Yaxian Yan and Jianhe Sun
Viruses 2019, 11(8), 715; https://0-doi-org.brum.beds.ac.uk/10.3390/v11080715 - 05 Aug 2019
Cited by 9 | Viewed by 3244
Abstract
Streptococcus suis (S. suis) is a gram-positive bacterium and zoonotic pathogen. Currently it poses a serious problem in the swine industry due to the emergence of antibiotic-resistant bacteria. Thus, novel antimicrobials against S. suis infections are urgently needed. In the previous [...] Read more.
Streptococcus suis (S. suis) is a gram-positive bacterium and zoonotic pathogen. Currently it poses a serious problem in the swine industry due to the emergence of antibiotic-resistant bacteria. Thus, novel antimicrobials against S. suis infections are urgently needed. In the previous study, a cell wall hydrolase or lysin derived from Streptococcus prophage phi5218, termed Ply5218, was identified. This lysin showed strong bacteriolytic activity against S. suis. In the current study, the in vitro data showed that after incubation with pig serum, the bacteriolytic efficacy of Ply5218 declined in a time-dependent manner. The in vivo assays indicated that a Ply5218 triple treatment (6, 24, and 48 h post infection) was effective against various serotypes of S. suis in a murine infection model. This regimen also alleviated streptococcal-induced clinical symptoms in piglets and significantly reduced the bacterial burden and levels of interleukin 6, a proinflammatory cytokine. This study indicates that Ply5218 shows strong antibacterial activity in pigs and has the potential to be used as a treatment for infectious diseases caused by S. suis. Full article
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20 pages, 3180 KiB  
Article
Expanding the Diversity of Myoviridae Phages Infecting Lactobacillus plantarum—A Novel Lineage of Lactobacillus Phages Comprising Five New Members
by Ifigeneia Kyrkou, Alexander Byth Carstens, Lea Ellegaard-Jensen, Witold Kot, Athanasios Zervas, Amaru Miranda Djurhuus, Horst Neve, Martin Hansen and Lars Hestbjerg Hansen
Viruses 2019, 11(7), 611; https://0-doi-org.brum.beds.ac.uk/10.3390/v11070611 - 04 Jul 2019
Cited by 16 | Viewed by 4635
Abstract
Lactobacillus plantarum is a bacterium with probiotic properties and promising applications in the food industry and agriculture. So far, bacteriophages of this bacterium have been moderately addressed. We examined the diversity of five new L. plantarum phages via whole genome shotgun sequencing and [...] Read more.
Lactobacillus plantarum is a bacterium with probiotic properties and promising applications in the food industry and agriculture. So far, bacteriophages of this bacterium have been moderately addressed. We examined the diversity of five new L. plantarum phages via whole genome shotgun sequencing and in silico protein predictions. Moreover, we looked into their phylogeny and their potential genomic similarities to other complete phage genome records through extensive nucleotide and protein comparisons. These analyses revealed a high degree of similarity among the five phages, which extended to the vast majority of predicted virion-associated proteins. Based on these, we selected one of the phages as a representative and performed transmission electron microscopy and structural protein sequencing tests. Overall, the results suggested that the five phages belong to the family Myoviridae, they have a long genome of 137,973–141,344 bp, a G/C content of 36.3–36.6% that is quite distinct from their host’s, and surprisingly, 7 to 15 tRNAs. Only an average 41/174 of their predicted genes were assigned a function. The comparative analyses unraveled considerable genetic diversity for the five L. plantarum phages in this study. Hence, the new genus “Semelevirus” was proposed, comprising exclusively of the five phages. This novel lineage of Lactobacillus phages provides further insight into the genetic heterogeneity of phages infecting Lactobacillus sp. The five new Lactobacillus phages have potential value for the development of more robust starters through, for example, the selection of mutants insensitive to phage infections. The five phages could also form part of phage cocktails, which producers would apply in different stages of L. plantarum fermentations in order to create a range of organoleptic outputs. Full article
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9 pages, 724 KiB  
Article
Unprecedented Diversity of Lactococcal Group 936 Bacteriophages Revealed by Amplicon Sequencing of the Portal Protein Gene
by Cyril Alexander Frantzen and Helge Holo
Viruses 2019, 11(5), 443; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050443 - 16 May 2019
Cited by 7 | Viewed by 2689
Abstract
Lactococcus lactis is one of the most important bacteria in dairy fermentations, being used in the production of cheese and buttermilk. The processes are vulnerable to phage attacks, and undefined mixtures of lactococcal strains are often used to reduce the risk of bacteriophage [...] Read more.
Lactococcus lactis is one of the most important bacteria in dairy fermentations, being used in the production of cheese and buttermilk. The processes are vulnerable to phage attacks, and undefined mixtures of lactococcal strains are often used to reduce the risk of bacteriophage caused fermentation failure. Other preventive measures include culture rotation to prevent phage build-up and phage monitoring. Phage diversity, rather than quantity, is the largest threat to fermentations using undefined mixed starter cultures. We have developed a method for culture independent diversity analysis of lytic bacteriophages of the 936 group, the phages most commonly found in dairies. Using, as a target, a highly variable region of the portal protein gene, we demonstrate an unprecedented diversity and the presence of new 936 phages in samples taken from cheese production. The method should be useful to the dairy industry and starter culture manufacturers in their efforts to reduce phage problems. Full article
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16 pages, 2800 KiB  
Article
Isolation and Characterization of Lactobacillus brevis Phages
by Marine Feyereisen, Jennifer Mahony, Gabriele A. Lugli, Marco Ventura, Horst Neve, Charles M. A. P. Franz, Jean-Paul Noben, Tadhg O’Sullivan and Douwe van Sinderen
Viruses 2019, 11(5), 393; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050393 - 26 Apr 2019
Cited by 20 | Viewed by 6038
Abstract
Lactobacillus brevis has been widely used in industry for fermentation purposes. However, it is also associated with the spoilage of foods and beverages, in particular, beer. There is an increasing demand for natural food preservation methods, and in this context, bacteriophages possess the [...] Read more.
Lactobacillus brevis has been widely used in industry for fermentation purposes. However, it is also associated with the spoilage of foods and beverages, in particular, beer. There is an increasing demand for natural food preservation methods, and in this context, bacteriophages possess the potential to control such spoilage bacteria. Just a few studies on phages infecting Lactobacillus brevis have been performed to date and in the present study, we report the isolation and characterization of five virulent phages capable of infecting Lb. brevis strains. The analysis reveals a high diversity among the isolates, with members belonging to both, the Myoviridae and Siphoviridae families. One isolate, designated phage 3-521, possesses a genome of 140.8 kb, thus representing the largest Lb. brevis phage genome sequenced to date. While the isolated phages do not propagate on Lb. brevis beer-spoiling strains, phages showed activity against these strains, impairing the growth of some Lb. brevis strains. The results highlight the potential of bacteriophage-based treatments as an effective approach to prevent bacterial spoilage of beer. Full article
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19 pages, 4191 KiB  
Article
A Cryptic Non-Inducible Prophage Confers Phage-Immunity on the Streptococcus thermophilus M17PTZA496
by Vinícius Da Silva Duarte, Sabrina Giaretta, Stefano Campanaro, Laura Treu, Andrea Armani, Armin Tarrah, Sérgio Oliveira de Paula, Alessio Giacomini and Viviana Corich
Viruses 2019, 11(1), 7; https://0-doi-org.brum.beds.ac.uk/10.3390/v11010007 - 22 Dec 2018
Cited by 21 | Viewed by 5318
Abstract
Streptococcus thermophilus is considered one of the most important species for the dairy industry. Due to their diffusion in dairy environments, bacteriophages can represent a threat to this widely used bacterial species. Despite the presence of a CRISPR-Cas system in the S. thermophilus [...] Read more.
Streptococcus thermophilus is considered one of the most important species for the dairy industry. Due to their diffusion in dairy environments, bacteriophages can represent a threat to this widely used bacterial species. Despite the presence of a CRISPR-Cas system in the S. thermophilus genome, some lysogenic strains harbor cryptic prophages that can increase the phage-host resistance defense. This characteristic was identified in the dairy strain S. thermophilus M17PTZA496, which contains two integrated prophages 51.8 and 28.3 Kb long, respectively. In the present study, defense mechanisms, such as a lipoprotein-encoding gene and Siphovirus Gp157, the last associated to the presence of a noncoding viral DNA element, were identified in the prophage M17PTZA496 genome. The ability to overexpress genes involved in these defense mechanisms under specific stressful conditions, such as phage attack, has been demonstrated. Despite the addition of increasing amounts of Mitomycin C, M17PTZA496 was found to be non-inducible. However, the transcriptional activity of the phage terminase large subunit was detected in the presence of the antagonist phage vB_SthS-VA460 and of Mitomycin C. The discovery of an additional immune mechanism, associated with bacteriophage-insensitive strains, is of utmost importance, for technological applications and industrial processes. To our knowledge, this is the first study reporting the capability of a prophage integrated into the S. thermophilus genome expressing different phage defense mechanisms. Bacteriophages are widespread entities that constantly threaten starter cultures in the dairy industry. In cheese and yogurt manufacturing, the lysis of Streptococcus thermophilus cultures by viral attacks can lead to huge economic losses. Nowadays S. thermophilus is considered a well-stablished model organism for the study of natural adaptive immunity (CRISPR-Cas) against phage and plasmids, however, the identification of novel bacteriophage-resistance mechanisms, in this species, is strongly desirable. Here, we demonstrated that the presence of a non-inducible prophage confers phage-immunity to an S. thermophilus strain, by the presence of ltp and a viral noncoding region. S. thermophilus M17PTZA496 arises as an unconventional model to study phage resistance and potentially represents an alternative starter strain for dairy productions. Full article
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12 pages, 3106 KiB  
Article
Unlocking the Potential of 46 New Bacteriophages for Biocontrol of Dickeya Solani
by Alexander B. Carstens, Amaru M. Djurhuus, Witold Kot, Deborah Jacobs-Sera, Graham F. Hatfull and Lars H. Hansen
Viruses 2018, 10(11), 621; https://0-doi-org.brum.beds.ac.uk/10.3390/v10110621 - 10 Nov 2018
Cited by 34 | Viewed by 4239
Abstract
Modern agriculture is expected to face an increasing global demand for food while also needing to comply with higher sustainability standards. Therefore, control of crop pathogens requires new, green alternatives to current methods. Potatoes are susceptible to several bacterial diseases, with infections by [...] Read more.
Modern agriculture is expected to face an increasing global demand for food while also needing to comply with higher sustainability standards. Therefore, control of crop pathogens requires new, green alternatives to current methods. Potatoes are susceptible to several bacterial diseases, with infections by soft rot Enterobacteriaceae (SRE) being a significant contributor to the major annual losses. As there are currently no efficient ways of combating SRE, we sought to develop an approach that could easily be incorporated into the potato production pipeline. To this end, 46 phages infecting the emerging potato pathogen Dickeya solani were isolated and thoroughly characterized. The 46 isolated phages were grouped into three different groups based on DNA similarity, representing two distinct clusters and a singleton. One cluster showed similarity to phages previously used to successfully treat soft rot in potatoes, whereas the remaining phages were novel and showed only very limited similarity to previously isolated phages. We selected six diverse phages in order to create the hereto most complex phage cocktail against SRE. The cocktail was applied in a proof-of-principle experiment to treat soft rot in potatoes under simulated storage conditions. We show that the phage cocktail was able to significantly reduce the incidence of soft rot as well as disease severity after 5 days of storage post-infection with Dickeya solani. This confirms results from previous studies that phages represent promising biocontrol agents against SRE infection in potato. Full article
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Review

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20 pages, 3602 KiB  
Review
Yersinia Phages and Food Safety
by Carlos G. Leon-Velarde, Jin Woo Jun and Mikael Skurnik
Viruses 2019, 11(12), 1105; https://0-doi-org.brum.beds.ac.uk/10.3390/v11121105 - 28 Nov 2019
Cited by 26 | Viewed by 6447
Abstract
One of the human- and animal-pathogenic species in genus Yersinia is Yersinia enterocolitica, a food-borne zoonotic pathogen that causes enteric infections, mesenteric lymphadenitis, and sometimes sequelae such as reactive arthritis and erythema nodosum. Y. enterocolitica is able to proliferate at 4 °C, [...] Read more.
One of the human- and animal-pathogenic species in genus Yersinia is Yersinia enterocolitica, a food-borne zoonotic pathogen that causes enteric infections, mesenteric lymphadenitis, and sometimes sequelae such as reactive arthritis and erythema nodosum. Y. enterocolitica is able to proliferate at 4 °C, making it dangerous if contaminated food products are stored under refrigeration. The most common source of Y. enterocolitica is raw pork meat. Microbiological detection of the bacteria from food products is hampered by its slow growth rate as other bacteria overgrow it. Bacteriophages can be exploited in several ways to increase food safety with regards to contamination by Y. enterocolitica. For example, Yersinia phages could be useful in keeping the contamination of food products under control, or, alternatively, the specificity of the phages could be exploited in developing rapid and sensitive diagnostic tools for the identification of the bacteria in food products. In this review, we will discuss the present state of the research on these topics. Full article
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26 pages, 2194 KiB  
Review
Understanding and Exploiting Phage–Host Interactions
by Edel Stone, Katrina Campbell, Irene Grant and Olivia McAuliffe
Viruses 2019, 11(6), 567; https://0-doi-org.brum.beds.ac.uk/10.3390/v11060567 - 18 Jun 2019
Cited by 107 | Viewed by 15670
Abstract
Initially described a century ago by William Twort and Felix d’Herelle, bacteriophages are bacterial viruses found ubiquitously in nature, located wherever their host cells are present. Translated literally, bacteriophage (phage) means ‘bacteria eater’. Phages interact and infect specific bacteria while not affecting other [...] Read more.
Initially described a century ago by William Twort and Felix d’Herelle, bacteriophages are bacterial viruses found ubiquitously in nature, located wherever their host cells are present. Translated literally, bacteriophage (phage) means ‘bacteria eater’. Phages interact and infect specific bacteria while not affecting other bacteria or cell lines of other organisms. Due to the specificity of these phage–host interactions, the relationship between phages and their host cells has been the topic of much research. The advances in phage biology research have led to the exploitation of these phage–host interactions and the application of phages in the agricultural and food industry. Phages may provide an alternative to the use of antibiotics, as it is well known that the emergence of antibiotic-resistant bacterial infections has become an epidemic in clinical settings. In agriculture, pre-harvest and/or post-harvest application of phages to crops may prevent the colonisation of bacteria that are detrimental to plant or human health. In addition, the abundance of data generated from genome sequencing has allowed the development of phage-derived bacterial detection systems of foodborne pathogens. This review aims to outline the specific interactions between phages and their host and how these interactions may be exploited and applied in the food industry. Full article
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28 pages, 325 KiB  
Review
Inactivation of Dairy Bacteriophages by Thermal and Chemical Treatments
by Mariángeles Briggiler Marcó, Viviana B. Suárez, Andrea Quiberoni and Silvina A. Pujato
Viruses 2019, 11(5), 480; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050480 - 25 May 2019
Cited by 18 | Viewed by 4126
Abstract
This article provides information on the characteristics of diverse phages of lactic acid bacteria and highlights the incidence of their presence in different dairy fermentations. As it is known, thermal treatments on raw milk and use of sanitizers in the disinfection of surfaces [...] Read more.
This article provides information on the characteristics of diverse phages of lactic acid bacteria and highlights the incidence of their presence in different dairy fermentations. As it is known, thermal treatments on raw milk and use of sanitizers in the disinfection of surfaces and equipment are strategies usually applied in dairy to prevent bacteriophage infections. In this sense, this review mainly focuses on the existing data about the resistance against thermal treatments and sanitizers usually used in the dairy industry worldwide, and the differences found among bacteriophages of diverse genera are remarked upon. Also, we provide information concerning the problems that have arisen as a consequence of the potential presence of bacteriophages in cheese whey powder and derivatives when they are added in fermented dairy product manufacturing. Finally, some important conclusions on each topic are marked and checkpoints to be considered are suggested. Full article
27 pages, 1924 KiB  
Review
Don’t Shut the Stable Door after the Phage Has Bolted—The Importance of Bacteriophage Inactivation in Food Environments
by Julia Sommer, Christoph Trautner, Anna Kristina Witte, Susanne Fister, Dagmar Schoder, Peter Rossmanith and Patrick-Julian Mester
Viruses 2019, 11(5), 468; https://0-doi-org.brum.beds.ac.uk/10.3390/v11050468 - 22 May 2019
Cited by 44 | Viewed by 8682
Abstract
In recent years, a new potential measure against foodborne pathogenic bacteria was rediscovered—bacteriophages. However, despite all their advantages, in connection to their widespread application in the food industry, negative consequences such as an uncontrolled phage spread as well as a development of phage [...] Read more.
In recent years, a new potential measure against foodborne pathogenic bacteria was rediscovered—bacteriophages. However, despite all their advantages, in connection to their widespread application in the food industry, negative consequences such as an uncontrolled phage spread as well as a development of phage resistant bacteria can occur. These problems are mostly a result of long-term persistence of phages in the food production environment. As this topic has been neglected so far, this article reviews the current knowledge regarding the effectiveness of disinfectant strategies for phage inactivation and removal. For this purpose, the main commercial phage products, as well as their application fields are first discussed in terms of applicable inactivation strategies and legal regulations. Secondly, an overview of the effectiveness of disinfectants for bacteriophage inactivation in general and commercial phages in particular is given. Finally, this review outlines a possible strategy for users of commercial phage products in order to improve the effectiveness of phage inactivation and removal after application. Full article
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