Bacteriophage Applications for Food Production and Processing
Abstract
:1. Introduction
2. Phage Biocontrol for Targeting Common Foodborne Bacterial Pathogens
2.1. Listeria monocytogenes
2.2. Salmonella spp.
2.3. Escherichia coli
2.4. Shigella spp.
2.5. Campylobacter jejuni
3. Bacteriophage Preparations as Commercial Products
3.1. Regulation of Bacteriophage Preparations
3.2. Challenges for Bacteriophage Biocontrol
3.2.1. Technical Challenges
3.2.2. Customer Acceptance
4. Concluding Remarks
Acknowledgments
Conflicts of Interest
References
- Havelaar, A.H.; Kirk, M.D.; Torgerson, P.R.; Gibb, H.J.; Hald, T.; Lake, R.J.; Praet, N.; Bellinger, D.C.; de Silva, N.R.; Gargouri, N.; et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med. 2015, 12, e1001923. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scharff, R.L. Economic burden from health losses due to foodborne illness in the United States. J. Food Prot. 2012, 75, 123–131. [Google Scholar] [CrossRef] [PubMed]
- Wolbang, C.M.; Fitos, J.L.; Treeby, M.T. The effect of high pressure processing on nutritional value and quality attributes of Cucumis melo L. Innov. Food Sci. Emerg. 2008, 9, 196–200. [Google Scholar] [CrossRef]
- Bajovic, B.; Bolumar, T.; Heinz, V. Quality considerations with high pressure processing of fresh and value added meat products. Meat Sci. 2012, 92, 280–289. [Google Scholar] [CrossRef] [PubMed]
- Suklim, K.; Flick, G.J.; Vichitphan, K. Effects of gamma irradiation on the physical and sensory quality and inactivation of Listeria monocytogenes in blue swimming crab meat (Portunas pelagicus). Radiat. Phys. Chem. 2014, 103, 22–26. [Google Scholar] [CrossRef]
- Wheeler, T.L.; Shackelford, S.D.; Koohmaraie, M. Trained sensory panel and consumer evaluation of the effects of gamma irradiation on palatability of vacuum-packaged frozen ground beef patties. J. Anim. Sci. 1999, 77, 3219–3224. [Google Scholar] [CrossRef] [PubMed]
- Beuchat, L.R.; Ryu, J.H. Produce handling and processing practices. Emerg. Infect. Dis. 1997, 3, 459–465. [Google Scholar] [CrossRef] [PubMed]
- Sohaib, M.; Anjum, F.M.; Arshad, M.S.; Rahman, U.U. Postharvest intervention technologies for safety enhancement of meat and meat based products; a critical review. J. Food Sci. Technol. 2016, 53, 19–30. [Google Scholar] [CrossRef] [PubMed]
- Sulakvelidze, A.; Alavidze, Z.; Morris, J.G., Jr. Bacteriophage therapy. Antimicrob. Agents Chemother. 2001, 45, 649–659. [Google Scholar] [CrossRef] [PubMed]
- Perera, M.N.; Abuladze, T.; Li, M.R.; Woolston, J.; Sulakvelidze, A. Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiol. 2015, 52, 42–48. [Google Scholar] [CrossRef] [PubMed]
- Viator, C.L.; Muth, M.K.; Brophy, J.E. Costs of Food Safety Investments; Report; RTI International: Research Triangle Park, NC, USA, 2015. Available online: https://www.fsis.usda.gov/wps/wcm/connect/0cdc568e-f6b1-45dc-88f1-45f343ed0bcd/Food-Safety-Costs.pdf?MOD=AJPERES (accessed on 19 March 2018).
- Sulakvelidze, A. Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogens. J. Sci. Food Agric. 2013, 93, 3137–3146. [Google Scholar] [CrossRef] [PubMed]
- Schmelcher, M.; Loessner, M.J. Bacteriophage endolysins: Applications for food safety. Curr. Opin. Biotechnol. 2016, 37, 76–87. [Google Scholar] [CrossRef] [PubMed]
- Greer, G.G. Bacteriophage control of foodborne bacteria. J. Food Prot. 2005, 68, 1102–1111. [Google Scholar] [CrossRef] [PubMed]
- Lone, A.; Anany, H.; Hakeem, M.; Aguis, L.; Avdjian, A.C.; Bouget, M.; Atashi, A.; Brovko, L.; Rochefort, D.; Griffiths, M.W. Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foods. Int. J. Food Microbiol. 2016, 217, 49–58. [Google Scholar] [CrossRef] [PubMed]
- Woolston, J.; Parks, A.R.; Abuladze, T.; Anderson, B.; Li, M.; Carter, C.; Hanna, L.F.; Heyse, S.; Charbonneau, D.; Sulakvelidze, A. Bacteriophages lytic for Salmonella rapidly reduce Salmonella contamination on glass and stainless steel surfaces. Bacteriophage 2013, 3, e25697. [Google Scholar] [CrossRef] [PubMed]
- Abuladze, T.; Li, M.; Menetrez, M.Y.; Dean, T.; Senecal, A.; Sulakvelidze, A. Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microbiol. 2008, 74, 6230–6238. [Google Scholar] [CrossRef] [PubMed]
- Woolston, J.; Sulakvelidze, A. Bacteriophages and food safety. In eLS; Chichester, Ed.; John Wiley & Sons Ltd.: Hoboken, NJ, USA, 2015. [Google Scholar]
- Endersen, L.; O’Mahony, J.; Hill, C.; Ross, R.P.; McAuliffe, O.; Coffey, A. Phage therapy in the food industry. Annu. Rev. Food Sci. Technol. 2014, 5, 327–349. [Google Scholar] [CrossRef] [PubMed]
- Bandara, N.; Jo, J.; Ryu, S.; Kim, K.P. Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Food Microbiol. 2012, 31, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Atterbury, R.J.; Connerton, P.L.; Dodd, C.E.; Rees, C.E.; Connerton, I.F. Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl. Environ. Microbiol. 2003, 69, 6302–6306. [Google Scholar] [CrossRef] [PubMed]
- Goode, D.; Allen, V.M.; Barrow, P.A. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 2003, 69, 5032–5036. [Google Scholar] [CrossRef] [PubMed]
- Bigwood, T.; Hudson, J.A.; Billington, C.; Carey-Smith, G.V.; Heinemann, J.A. Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiol. 2008, 25, 400–406. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.P.; Klumpp, J.; Loessner, M.J. Enterobacter sakazakii bacteriophages can prevent bacterial growth in reconstituted infant formula. Int. J. Food Microbiol. 2007, 115, 195–203. [Google Scholar] [CrossRef] [PubMed]
- Zuber, S.; Boissin-Delaporte, C.; Michot, L.; Iversen, C.; Diep, B.; Brussow, H.; Breeuwer, P. Decreasing Enterobacter sakazakii (Cronobacter spp.) food contamination level with bacteriophages: Prospects and problems. Microb. Biotechnol. 2008, 1, 532–543. [Google Scholar] [CrossRef] [PubMed]
- O’Flynn, G.; Ross, R.P.; Fitzgerald, G.F.; Coffey, A. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 2004, 70, 3417–3424. [Google Scholar] [CrossRef] [PubMed]
- Sharma, M.; Patel, J.R.; Conway, W.S.; Ferguson, S.; Sulakvelidze, A. Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettuce. J. Food Prot. 2009, 72, 1481–1485. [Google Scholar] [CrossRef] [PubMed]
- Viazis, S.; Akhtar, M.; Feirtag, J.; Diez-Gonzalez, F. Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol. 2011, 28, 149–157. [Google Scholar] [CrossRef] [PubMed]
- Carter, C.D.; Parks, A.; Abuladze, T.; Li, M.; Woolston, J.; Magnone, J.; Senecal, A.; Kropinski, A.M.; Sulakvelidze, A. Bacteriophage cocktail significantly reduces Escherichia coli O157:H7 contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage 2012, 2, 178–185. [Google Scholar] [CrossRef] [PubMed]
- Boyacioglu, O.; Sharma, M.; Sulakvelidze, A.; Goktepe, I. Biocontrol of Escherichia coli O157:H7 on fresh-cut leafy greens. Bacteriophage 2013, 3, e24620. [Google Scholar] [CrossRef] [PubMed]
- Hudson, J.A.; Billington, C.; Wilson, T.; On, S.L. Effect of phage and host concentration on the inactivation of Escherichia coli O157:H7 on cooked and raw beef. Food Sci. Technol. Int. 2013, 21, 104–109. [Google Scholar] [CrossRef] [PubMed]
- Ferguson, S.; Roberts, C.; Handy, E.; Sharma, M. Lytic bacteriophages reduce Escherichia coli O157:H7 on fresh cut lettuce introduced through cross-contamination. Bacteriophage 2013, 3, e24323. [Google Scholar] [CrossRef] [PubMed]
- McLean, S.K.; Dunn, L.A.; Palombo, E.A. Phage inhibition of Escherichia coli in ultrahigh-temperature-treated and raw milk. Foodborne Pathog. Dis. 2013, 10, 956–962. [Google Scholar] [CrossRef] [PubMed]
- Magnone, J.P.; Marek, P.J.; Sulakvelidze, A.; Senecal, A.G. Additive approach for inactivation of Escherichia coli O157:H7, Salmonella, and Shigella spp. on contaminated fresh fruits and vegetables using bacteriophage cocktail and produce wash. J. Food Prot. 2013, 76, 1336–1341. [Google Scholar] [CrossRef] [PubMed]
- Leverentz, B.; Conway, W.S.; Camp, M.J.; Janisiewicz, W.J.; Abuladze, T.; Yang, M.; Saftner, R.; Sulakvelidze, A. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microbiol. 2003, 69, 4519–4526. [Google Scholar] [CrossRef] [PubMed]
- Leverentz, B.; Conway, W.S.; Janisiewicz, W.; Camp, M.J. Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. J. Food Prot. 2004, 67, 1682–1686. [Google Scholar] [CrossRef] [PubMed]
- Carlton, R.M.; Noordman, W.H.; Biswas, B.; de Meester, E.D.; Loessner, M.J. Bacteriophage P100 for control of Listeria monocytogenes in foods: Genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharmacol. 2005, 43, 301–312. [Google Scholar] [CrossRef] [PubMed]
- Guenther, S.; Huwyler, D.; Richard, S.; Loessner, M.J. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microbiol. 2009, 75, 93–100. [Google Scholar] [CrossRef] [PubMed]
- Soni, K.A.; Nannapaneni, R. Bacteriophage significantly reduces Listeria monocytogenes on raw salmon fillet tissue. J. Food Prot. 2010, 73, 32–38. [Google Scholar] [CrossRef] [PubMed]
- Soni, K.A.; Nannapaneni, R.; Hagens, S. Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage Listex P100. Foodborne Pathog. Dis. 2010, 7, 427–434. [Google Scholar] [CrossRef] [PubMed]
- Guenther, S.; Loessner, M.J. Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses. Bacteriophage 2011, 1, 94–100. [Google Scholar] [CrossRef] [PubMed]
- Bigot, B.; Lee, W.J.; McIntyre, L.; Wilson, T.; Hudson, J.A.; Billington, C.; Heinemann, J.A. Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage. Food Microbiol. 2011, 28, 1448–1452. [Google Scholar] [CrossRef] [PubMed]
- Soni, K.A.; Desai, M.; Oladunjoye, A.; Skrobot, F.; Nannapaneni, R. Reduction of Listeria monocytogenes in queso fresco cheese by a combination of listericidal and listeriostatic GRAS antimicrobials. Int. J. Food Microbiol. 2012, 155, 82–88. [Google Scholar] [CrossRef] [PubMed]
- Chibeu, A.; Agius, L.; Gao, A.; Sabour, P.M.; Kropinski, A.M.; Balamurugan, S. Efficacy of bacteriophage LISTEXTM P100 combined with chemical antimicrobials in reducing Listeria monocytogenes in cooked turkey and roast beef. Int. J. Food Microbiol. 2013, 167, 208–214. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, M.; Viñas, I.; Colàs, P.; Anguera, M.; Usall, J.; Abadias, M. Effectiveness of a bacteriophage in reducing Listeria monocytogenes on fresh-cut fruits and fruit juices. Food Microbiol. 2014, 38, 137–142. [Google Scholar] [CrossRef] [PubMed]
- Silva, E.N.; Figueiredo, A.C.; Miranda, F.A.; de Castro Almeida, R.C. Control of Listeria monocytogenes growth in soft cheeses by bacteriophage P100. Braz. J. Microbiol. 2014, 45, 11–16. [Google Scholar] [CrossRef] [PubMed]
- Figueiredo, A.C.L.; Almeida, R.C.C. Antibacterial efficacy of nisin, bacteriophage P100 and sodium lactate against Listeria monocytogenes in ready-to-eat sliced pork ham. Braz. J. Microbiol. 2017, 48, 724–729. [Google Scholar] [CrossRef] [PubMed]
- Endersen, L.; Coffey, A.; Neve, H.; McAuliffe, O.; Ross, R.P.; O’Mahony, J.M. Isolation and characterisation of six novel mycobacteriophages and investigation of their antimicrobial potential in milk. Int. Dairy J. 2013, 28, 8–14. [Google Scholar] [CrossRef]
- Modi, R.; Hirvi, Y.; Hill, A.; Griffiths, M.W. Effect of phage on survival of Salmonella Enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J. Food Prot. 2001, 64, 927–933. [Google Scholar] [CrossRef] [PubMed]
- Leverentz, B.; Conway, W.S.; Alavidze, Z.; Janisiewicz, W.J.; Fuchs, Y.; Camp, M.J.; Chighladze, E.; Sulakvelidze, A. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: A model study. J. Food Prot. 2001, 64, 1116–1121. [Google Scholar] [CrossRef] [PubMed]
- Whichard, J.M.; Sriranganathan, N.; Pierson, F.W. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J. Food Prot. 2003, 66, 220–225. [Google Scholar] [CrossRef] [PubMed]
- Higgins, J.P.; Higgins, S.E.; Guenther, K.L.; Huff, W.; Donoghue, A.M.; Donoghue, D.J.; Hargis, B.M. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult. Sci. 2005, 84, 1141–1145. [Google Scholar] [CrossRef] [PubMed]
- Ye, J.; Kostrzynska, M.; Dunfield, K.; Warriner, K. Control of Salmonella on sprouting mung bean and alfalfa seeds by using a biocontrol preparation based on antagonistic bacteria and lytic bacteriophages. J. Food Prot. 2010, 73, 9–17. [Google Scholar] [CrossRef] [PubMed]
- Guenther, S.; Herzig, O.; Fieseler, L.; Klumpp, J.; Loessner, M.J. Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int. J. Food Microbiol. 2012, 154, 66–72. [Google Scholar] [CrossRef] [PubMed]
- Spricigo, D.A.; Bardina, C.; Cortes, P.; Llagostera, M. Use of a bacteriophage cocktail to control Salmonella in food and the food industry. Int. J. Food Microbiol. 2013, 165, 169–174. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.W.; Kim, J.W.; Jung, T.S.; Woo, G.J. wksl3, a new biocontrol agent for Salmonella enterica serovars Enteritidis and Typhimurium in foods: Characterization, application, sequence analysis, and oral acute toxicity study. Appl. Environ. Microbiol. 2013, 79, 1956–1968. [Google Scholar] [CrossRef] [PubMed]
- Hungaro, H.M.; Mendonça, R.C.S.; Gouvêa, D.M.; Vanetti, M.C.D.; Pinto, C.L.D. Use of bacteriophages to reduce Salmonella in chicken skin in comparison with chemical agents. Food Res. Int. 2013, 52, 75–81. [Google Scholar] [CrossRef]
- Zinno, P.; Devirgiliis, C.; Ercolini, D.; Ongeng, D.; Mauriello, G. Bacteriophage P22 to challenge Salmonella in foods. Int. J. Food Microbiol. 2014, 191, 69–74. [Google Scholar] [CrossRef] [PubMed]
- Sukumaran, A.T.; Nannapaneni, R.; Kiess, A.; Sharma, C.S. Reduction of Salmonella on chicken meat and chicken skin by combined or sequential application of lytic bacteriophage with chemical antimicrobials. Int. J. Food Microbiol. 2015, 207, 8–15. [Google Scholar] [CrossRef] [PubMed]
- Sukumaran, A.T.; Nannapaneni, R.; Kiess, A.; Sharma, C.S. Reduction of Salmonella on chicken breast fillets stored under aerobic or modified atmosphere packaging by the application of lytic bacteriophage preparation SalmoFreshTM. Poult. Sci. 2016, 95, 668–675. [Google Scholar] [CrossRef] [PubMed]
- Soffer, N.; Abuladze, T.; Woolston, J.; Li, M.; Hanna, L.F.; Heyse, S.; Charbonneau, D.; Sulakvelidze, A. Bacteriophages safely reduce Salmonella contamination in pet food and raw pet food ingredients. Bacteriophage 2016, 6, e1220347. [Google Scholar] [CrossRef] [PubMed]
- Hong, Y.; Schmidt, K.; Marks, D.; Hatter, S.; Marshall, A.; Albino, L.; Ebner, P. Treatment of Salmonella-contaminated eggs and pork with a broad-spectrum, single bacteriophage: Assessment of efficacy and resistance development. Foodborne Pathog. Dis. 2016, 13, 679–688. [Google Scholar] [CrossRef] [PubMed]
- Grant, A.; Parveen, S.; Schwarz, J.; Hashem, F.; Vimini, B. Reduction of Salmonella in ground chicken using a bacteriophage. Poult. Sci. 2017, 96, 2845–2852. [Google Scholar] [CrossRef] [PubMed]
- Yeh, Y.; de Moura, F.H.; Van Den Broek, K.; de Mello, A.S. Effect of ultraviolet light, organic acids, and bacteriophage on Salmonella populations in ground beef. Meat Sci. 2018, 139, 44–48. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Wang, R.; Bao, H.D. Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poult. Sci. 2013, 92, 211–217. [Google Scholar] [CrossRef] [PubMed]
- Soffer, N.; Woolston, J.; Li, M.; Das, C.; Sulakvelidze, A. Bacteriophage preparation lytic for Shigella significantly reduces Shigella sonnei contamination in various foods. PLoS ONE 2017, 12, e0175256. [Google Scholar] [CrossRef] [PubMed]
- Garcia, P.; Madera, C.; Martinez, B.; Rodriguez, A. Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. Int. Dairy J. 2007, 17, 1232–1239. [Google Scholar] [CrossRef]
- Bueno, E.; García, P.; Martínez, B.; Rodríguez, A. Phage inactivation of Staphylococcus aureus in fresh and hard-type cheeses. Int. J. Food Microbiol. 2012, 158, 23–27. [Google Scholar] [CrossRef] [PubMed]
- Mai, V.; Ukhanova, M.; Reinhard, M.K.; Li, M.; Sulakvelidze, A. Bacteriophage administration significantly reduces Shigella colonization and shedding by Shigella-challenged mice without deleterious side effects and distortions in the gut microbiota. Bacteriophage 2015, 5, e1088124. [Google Scholar] [CrossRef] [PubMed]
- Tokman, J.I.; Kent, D.J.; Wiedmann, M.; Denes, T. Temperature significantly affects the plaguing and adsorption efficiencies of Listeria phages. Front Microbiol. 2016, 7, 631. [Google Scholar] [CrossRef] [PubMed]
- Hoskisson, P.A.; Smith, M.C. Hypervariation and phase variation in the bacteriophage ‘resistome’. Curr. Opin. Microbiol. 2007, 10, 396–400. [Google Scholar] [CrossRef] [PubMed]
- Freeman, L.M.; Chandler, M.L.; Hamper, B.A.; Weeth, L.P. Current knowledge about the risks and benefits of raw meat-based diets for dogs and cats. J. Am. Vet. Med. Assoc. 2013, 243, 1549–1558. [Google Scholar] [CrossRef] [PubMed]
- Behravesh, C.B.; Ferraro, A.; Deasy, M., 3rd; Dato, V.; Moll, M.; Sandt, C.; Rea, N.K.; Rickert, R.; Marriott, C.; Warren, K.; et al. Human Salmonella infections linked to contaminated dry dog and cat food, 2006–2008. Pediatrics 2010, 126, 477–483. [Google Scholar] [CrossRef] [PubMed]
- Heyse, S.; Hanna, L.F.; Woolston, J.; Sulakvelidze, A.; Charbonneau, D. Bacteriophage cocktail for biocontrol of Salmonella in dried pet food. J. Food Prot. 2015, 78, 97–103. [Google Scholar] [CrossRef] [PubMed]
- Snyder, A.B.; Perry, J.J.; Yousef, A.E. Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce. Int. J. Food Microbiol. 2016, 236, 90–97. [Google Scholar] [CrossRef] [PubMed]
- Tomat, D.; Quiberoni, A.; Mercanti, D.; Balagué, C. Hard surfaces decontamination of enteropathogenic and Shiga toxin-producing Escherichia coli using bacteriophages. Food Res. Int. 2014, 57, 123–129. [Google Scholar] [CrossRef]
- Bower, C.K.; Daeschel, M.A. Resistance responses of microorganisms in food environments. Int. J. Food Microbiol. 1999, 50, 33–44. [Google Scholar] [CrossRef]
- Kotloff, K.L.; Winickoff, J.P.; Ivanoff, B.; Clemens, J.D.; Swerdlow, D.L.; Sansonetti, P.J.; Adak, G.K.; Levine, M.M. Global burden of Shigella infections: Implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 1999, 77, 651–666. [Google Scholar] [PubMed]
- Firlieyanti, A.S.; Connerton, P.L.; Connerton, I.F. Campylobacters and their bacteriophages from chicken liver: The prospect for phage biocontrol. Int. J. Food Microbiol. 2016, 237, 121–127. [Google Scholar] [CrossRef] [PubMed]
- Hammerl, J.A.; Jäckel, C.; Alter, T.; Janzcyk, P.; Stingl, K.; Knüver, M.T.; Hertwig, S. Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLoS ONE 2014, 9, e114785. [Google Scholar] [CrossRef] [PubMed]
- Zampara, A.; Sørensen, M.C.H.; Elsser-Gravesen, A.; Brøndsted, L. Significance of phage-host interactions for biocontrol of Campylobacter jejuni in food. Food Control. 2017, 73, 1169–1175. [Google Scholar] [CrossRef]
- Kittler, S.; Fischer, S.; Abdulmawjood, A.; Glunder, G.; Klein, G. Effect of bacteriophage application on Campylobacter jejuni loads in commercial broiler flocks. Appl. Environ. Microbiol. 2013, 79, 7525–7533. [Google Scholar] [CrossRef] [PubMed]
- Sorensen, M.C.; Gencay, Y.E.; Birk, T.; Baldvinsson, S.B.; Jackel, C.; Hammerl, J.A.; Vegge, C.S.; Neve, H.; Brondsted, L. Primary isolation strain determines both phage type and receptors recognised by Campylobacter jejuni bacteriophages. PLoS ONE 2015, 10, e0116287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hudson, J.A.; McIntyre, L.; Billington, C. Application of bacteriophages to control pathogenic and spoilage bacteria in food processing and distribution. In Bacteriophages in the Control of Food- and Waterborne Pathogens; Sabour, P.M., Griffiths, M.W., Eds.; ASM Press: Washington, DC, USA, 2010; pp. 119–135. [Google Scholar]
- US Food and Drug Administration Center for Food Safety and Applied Nutrition (FDA). Quantitative Assessment of Relative Risk to Public Health from Foodborne Listeria Monocytogenes Among Selected Categories of Ready-to-Eat Foods; US Food and Drug Administration Center for Food Safety and Applied Nutrition: College Park, MD, USA, 2003. Available online: https://www.fda.gov/downloads/food/scienceresearch/researchareas/riskassessmentsafetyassessment/ucm197330.pdf (accessed on 19 March 2018).
- Rodríguez, E.; Seguer, J.; Rocabayera, X.; Manresa, A. Cellular effects of monohydrochloride of l-arginine, Nα-lauroyl ethylester (LAE) on exposure to Salmonella typhimurium and Staphylococcus aureus. J. Appl. Microbiol. 2004, 96, 903–912. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Li, L.; Zhao, Z.; Peng, D.; Zhou, X. Polar flagella rotation in Vibrio parahaemolyticus confers resistance to bacteriophage infection. Sci. Rep. 2016, 6, 26147. [Google Scholar] [CrossRef] [PubMed]
- Marti, R.; Zurfluh, K.; Hagens, S.; Pianezzi, J.; Klumpp, J.; Loessner, M.J. Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC. Mol. Microbiol. 2013, 87, 818–834. [Google Scholar] [CrossRef] [PubMed]
- Lindberg, A.A.; Holme, T. Influence of O side chains on the attachment of the Felix O-1 bacteriophage to Salmonella bacteria. J. Bacteriol. 1969, 99, 513–519. [Google Scholar] [PubMed]
- Reganold, J.P.; Wachter, J.M. Organic agriculture in the twenty-first century. Nat. Plants 2016, 2, 15221. [Google Scholar] [CrossRef] [PubMed]
- Woods, T.; Ernst, M.; Tropp, D. Community Supported Agriculture–New Models for Changing Markets; U.S. Department of Agriculture, Agricultural Marketing Service: Washington, DC, USA, 2017.
- Hatfull, G.F. Bacteriophage genomics. Curr. Opin. Microbiol. 2008, 11, 447–453. [Google Scholar] [CrossRef] [PubMed]
- Dalmasso, M.; Hill, C.; Ross, R.P. Exploiting gut bacteriophages for human health. Trends Microbiol. 2014, 22, 399–405. [Google Scholar] [CrossRef] [PubMed]
- Sulakvelidze, A.; Barrow, P. Phage therapy in animals and agribusiness. In Bacteriophages: Biology and Applications; Kutter, E., Sulakvelidze, A., Eds.; CRC Press: Boca Raton, FL, USA, 2005; pp. 335–380. [Google Scholar]
- Suárez, V.B.; Quiberoni, A.; Binetti, A.G.; Reinheimer, J.A. Thermophilic lactic acid bacteria phages isolated from Argentinian dairy industries. J. Food Prot. 2002, 65, 1597–1604. [Google Scholar] [CrossRef] [PubMed]
- Gautier, M.; Rouault, A.; Sommer, P.; Briandet, R. Occurrence of Propionibacterium freudenreichii bacteriophages in swiss cheese. Appl. Environ. Microbiol. 1995, 61, 2572–2576. [Google Scholar] [PubMed]
- Naanwaab, C.; Yeboah, O.A.; Ofori Kyei, F.; Sulakvelidze, A.; Goktepe, I. Evaluation of consumers’ perception and willingness to pay for bacteriophage treated fresh produce. Bacteriophage 2014, 4, e979662. [Google Scholar] [CrossRef] [PubMed]
Bacterium * | Phages | Notes | Ref. |
---|---|---|---|
Bacillus cereus | BCP1-1 | Bacillus cereus counts decreased after treatment with a single phage in fermented soya bean paste without affecting Bacillus subtilis, a critical component of the fermentation process. | [20] |
Campylobacter jejuni | Φ2 | Counts of Campylobacter were reduced by ~1 log on the surface of chicken skin stored at 4 °C after the application of a single phage. | [21] |
Campylobacter jejuni; Salmonella spp. | C. jejuni typing page 12673, P22, 29C; Salmonella typing phage 12 | C. jejuni levels decreased ~2 logs on experimentally-contaminated chicken skin after application of phage at a MOI of 100:1 or 1000:1. Salmonella levels were reduced by ~2 logs on chicken skin treated with phage at an MOI of either 100:1 or 1000:1 and stored for 48 h; bacterial counts were reduced below the limit of detection when lower levels of bacteria were used to contaminate the chicken. | [22] |
Campylobacter jejuni; Salmonella spp. | Cj6; P7 | Campylobacter levels significantly decreased in beef after application of the phage Cj6, and decreases in bacterial levels were not significant at low levels of bacterial contamination (~100 CFU/cm2). Salmonella counts were decreased ~2–3 logs at 5 °C and >5.9 logs at 24 °C in raw and cooked beef after P7 phage application. Surviving Salmonella colonies were still sensitive to P7. For both phages, the killing of bacteria was higher at an MOI of 10,000:1 and ~10,000 CFU/cm2 of bacteria. | [23] |
Cronobacter sakazakii | ESP 1-3, ESP 732-1 | In infant formula, Cronobacter sakazakii (formerly Enterobacter sakazakii) levels were decreased after phage addition. The reduction was dependent on the phage concentration, and the phages were more effective at 24 °C than 37 °C or 12 °C. | [24] |
Cronobacter sakazakii | Five phages | Growth of 36 of 40 test strains was inhibited by a phage cocktail tested in infant formula experimentally contaminated with C. sakazakii. Furthermore, both high and low concentrations (106 and 102 CFU/mL) of bacteria were eliminated from liquid culture medium treated with the individual phage (108 PFU/mL). | [25] |
Escherichia coli O157:H7 | e11/2, pp01, e4/1c | After incubation at 37 °C, a three-phage cocktail used to treat the surface of beef that was contaminated (103 CFU/g) with E. coli O157:H7 eliminated the bacterium from a majority of the treated specimens. | [26] |
Escherichia coli O157:H7 | EcoShield™ (formerly ECP-100) | E. coli 0157:H7 levels decreased by ~1–3 logs, or were reduced below the limits of detection, on tomatoes, broccoli or spinach after treatment with a phage cocktail, while E. coli O157:H7 levels were decreased by ~1 log when the phages were applied to ground beef. | [17] |
Escherichia coli O157:H7 | EcoShield™ (formerly ECP-100) | A phage cocktail applied to experimentally contaminated lettuce and cut cantaloupe significantly reduced E. coli O157:H7 levels by up to 1.9 and 2.5 logs, respectively. | [27] |
Escherichia coli O157:H7 | Cocktail BEC8 | At various temperatures (4, 8, 23 and 37 °C), the phage cocktail significantly reduced the level of E. coli O157:H7 on leafy green vegetables by ~2–4 logs. The inclusion of an essential oil (trans-cinnamaldehyde) increased this effect. | [28] |
Escherichia coli O157:H7 | EcoShield™ (formerly ECP-100) | The levels of E. coli O157:H7 were reduced by ≥94% and ~87% on the surface of experimentally contaminated beef and lettuce, respectively, after addition of the phage cocktail; however, the single treatment did not protect foods after recontamination with the same bacteria (i.e., phage biocontrol had no continued technical effect on the foods). | [29] |
Escherichia coli O157:H7 | EcoShield™ (formerly ECP-100) | After a 30 min phage treatment at both 4 and 10 °C, levels of E. coli O157:H7 decreased by >2 logs on leafy greens under both ambient and modified atmosphere packaging storage. | [30] |
Escherichia coli | FAHEc1 | Contamination of raw and cooked beef decreased by 2–4 logs at 5, 24 and 37 °C in a concentration dependent manner after phage application. The E. coli displayed regrowth at higher temperatures. | [31] |
Escherichia coli O157:H7 | EcoShield™ (formerly ECP-100) | A phage cocktail was applied to lettuce by spraying and dipping. A larger initial reduction (~0.8–1.3 logs) in E. coli O157:H7 counts was observed after spraying. Dipping required submerging the lettuce for as long as 2 min, and the initial reductions were not significant. After 1 day of storage at 4 °C, dipping in the highest concentration of the phage cocktail reduced E. coli by ~0.7 log. | [32] |
Escherichia coli | EC6, EC9, EC11 | Two E. coli strains were eradicated from raw and UHT milk after treatment with a three-phage cocktail at 5–9 °C and 25 °C. For a third E. coli strain, phage treatment eliminated the bacteria from UHT milk; however, after an initial reduction, regrowth occurred in the raw milk after 144 or 9 h for 5–9 °C and 25 °C storage, respectively. | [33] |
Escherichia coli, Salmonella, Shigella | EcoShield™ (formerly ECP-100), SalmoFresh™, ShigActive™ | Phage cocktails were as effective or more effective than chlorine wash at reducing targeted pathogenic bacteria from broccoli, cantaloupe and strawberries in samples containing a large amount of organic content. Combination of the phage cocktail and a produce wash generated a synergistic effect, i.e., higher reductions of bacteria. | [34] |
Listeria monocytogenes | ListShield™ (formerly LMP-102) | Listeria counts decreased by ~2 logs and ~0.4 log after application of a phage cocktail on melon and apple slices, respectively; a synergistic effect was observed when phage and nisin were used, decreasing levels of Listeria on the fruit ~5.7 logs and ~2.3 logs, respectively. | [35] |
Listeria monocytogenes | ListShield™ (formerly LMP-102) | Application of a phage cocktail 1, 0.5 or 0 h before honeydew melon tissue were contaminated with the bacterium was most effective at reducing Listeria counts. This effect depended on the concentration of phage applied. Listeria counts decreased by ~5–7 logs after 7 days, when the phages were applied at the times described above. | [36] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Levels of Listeria were reduced by at least 3.5 logs after a single phage was administered to the surface of ripened red-smear soft cheese. The surviving Listeria colonies isolated from the cheese after phage treatment were not resistant to the phage. | [37] |
Listeria monocytogenes | A511, PhageGuard Listex™ (formerly Listex™; P100) | Levels of Listeria in experimentally contaminated chocolate milk and mozzarella cheese brine were eradicated after phage treatment at 6 °C. When the phage cocktail was applied to various solid foods, including sliced cabbage, iceberg lettuce leaves, smoked salmon, mixed seafood, hot dogs, and sliced turkey meat, a reduction of Listeria of up to 5 logs was observed. | [38] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Listeria counts decreased by 1.8–3.5 logs after application of a single phage at ~108 PFU/g to the surface of raw salmon fillets that were stored at 4 °C or 22 °C. | [39] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Levels of Listeria decreased by 1.4–2.0 logs CFU/g at 4 °C, 1.7–2.1 logs CFU/g at 10 °C, and 1.6–2.3 logs CFU/g at room temperature (22 °C) after application a single phage to the surface of raw catfish fillets. Regrowth was not observed after ten days of storage at either 4 °C or 10 °C. | [40] |
Listeria monocytogenes | A511 | The natural microbial community on soft cheese was maintained after addition of the phage. Levels of Listeria on experimentally contaminated cheese decreased by 2 logs and additional phage administrations did not improve the reduction of Listeria. | [41] |
Listeria monocytogenes | FWLLm1 | Listeria levels decreased by 1–2 logs on the surface of experimentally contaminated chicken stored in vacuum packages at 4 °C or 30 °C. Subsequent regrowth of Listeria was observed at 30 °C, but not at 4 °C. | [42] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Counts of Listeria decreased by ~3 logs in experimentally contaminated queso fresco cheese after the addition of a single phage; however, subsequent growth was observed. Regrowth was prevented, and a similar log reduction was observed when PL + SD were included with the phage. Reduction of Listeria was lower, and regrowth occurred when LAE was included with phage. | [43] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Compared to PL or PL + SD, a single phage was most effective at decreasing Listeria levels on RTE roast beef and turkey after storage at 4 °C or 10 °C, and subsequent bacterial growth was observed at both temperatures. Similar log reductions occurred when PL or PL + SD were used in conjunction with the phage, and regrowth was prevented or diminished at both 4 °C and 10 °C. | [44] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Counts of Listeria decreased by ~1.5 logs on experimentally contaminated melon and pear slices, but not apple slices after two days at 10 °C. Additionally, treatment with phage did not impact Listeria levels in apple juice but decreased bacterial contamination by ~4 and ~2.5 logs in melon and pear juice, respectively. | [45] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | Listeria levels on soft cheese decreased by ~2–3 logs after 30 min and ~0.8–1 log after storage for 7 days at 10 °C. | [46] |
Listeria monocytogenes | ListShield™ (formerly LMP-102) | Counts of Listeria decreased by 0.7 and 1.1 log on experimentally contaminated cheese and lettuce, respectively, after a 5 min treatment with phage and decreased the bacteria 1.1 log on the surface of apple slices after 24 h when combined with an antibrowning solution. The phage cocktail also virtually eliminated Listeria from experimentally contaminated frozen entrees that were frozen and thawed after treatment and was effective at eliminating environmental contamination by Listeria at a smoked salmon preparation plant. | [10] |
Listeria monocytogenes | PhageGuard Listex™ (formerly Listex™; P100) | When applied to the surface of experimentally contaminated sliced pork ham, the phage reduced Listeria counts below the limit of detection after 72 h, and performed better than nisin, sodium lactate, or combinations of these antibacterial measures. | [47] |
Mycobacterium smegmatis | Six phages | M. smegmatis counts were reduced below the limit of detection in milk treated with a six-phage cocktail or each component phage. Subsequent bacterial growth occurred when the component phages were used, but no growth was observed after 96 h at 37 °C, when the cocktail was applied. | [48] |
Salmonella spp. | SJ2 | Salmonella levels were reduced by 1–2 logs in raw and pasteurized cheeses created using milk that was treated with phage, while cheese made from milk without phage saw Salmonella counts rise ~1 log. | [49] |
Salmonella spp. | SCPLX-1 | Counts of Salmonella decreased by ~3.5 logs at 5 and 10 °C and ~2.5 logs at 20 °C on melon slices after application of a four-phage cocktail; treatment of apple slices with phage showed no reduction of bacteria. | [50] |
Salmonella spp. | Felix-O1 | Salmonella counts decreased by 1.8–2.1 logs after phage application to chicken frankfurters. | [51] |
Salmonella spp. | PHL4 | The levels of Salmonella recovered from experimentally contaminated broiler and naturally contaminated turkey carcasses were reduced by as high as 100% or 60%, respectively, after phage administration. | [52] |
Salmonella spp. | Levels of Salmonella decreased by ~3 logs after application of a phage cocktail to sprouts; addition of an antagonistic bacteria to the phage cocktail increased this reduction to ~6 logs. | [53] | |
Salmonella spp. | FO1-E2 | ln chocolate milk and mixed seafood, Salmonella levels were reduced to undetectable levels after phage treatment and storage for 24 h at 8 °C and remained below the limit of detection. When foods were phage-treated and stored at 15 °C, Salmonella counts were reduced to undetectable levels within 24–48 h for hot dogs, sliced turkey breast, and chocolate milk, but regrowth occurred after 5 days. Salmonella levels were initially inhibited at ~0.5–2 logs and ~1–3 logs in egg yolk and mixed seafood, respectively, after phage addition; but bacterial recovery matched controls in egg yolks after two days, while the log reduction was maintained in seafood. | [54] |
Salmonella spp. | UAB_Phi 20, UAB_Phi78, UAB_Phi87 | Salmonella counts decreased by ~1 log on the shells of fresh eggs and by 2–4 logs on lettuce 60 min after application of the phage. After an initial reduction of 1–2 logs, when chicken breasts were dipped in a phage cocktail, no further decrease in the bacterial counts was observed over the next seven days at 4 °C. The levels of Salmonella were reduced by 2–4 logs on pig skin after phage application and storage for 6 h at 33 °C. | [55] |
Salmonella spp. | wksl3 | Salmonella counts decreased by ~3 logs on chicken skin after application of a single phage, and no further decrease in bacterial levels was observed over the next seven days at 8 °C. Further, mice that received a single dose of phage orally displayed no adverse effects. | [56] |
Salmonella spp. | Five phages | The levels of Salmonella decreased by ~1 log on chicken skin after application of a five-phage cocktail comprised of closely related phages. The reduction of bacteria achieved by the phages was comparable to three different chemical antimicrobials. | [57] |
Salmonella spp. | P22 | After the administration of a single temperate phage and storage at 4 °C, levels of Salmonella decreased by ~0.5–2 logs on chicken, below the limits of detection in whole and skimmed milk, ~3 logs in apple juice, ~2 logs in liquid egg, and ~2 logs in an energy drink. | [58] |
Salmonella spp. | SalmoFresh™ | The stability of a Salmonella-specific phage preparation was determined in various chemical antimicrobials. Treatment of chicken breast fillets with a combination of phages and individual chemical antimicrobials did not produce a synergistic effect on the reduction of Salmonella; however, application of chlorine or PAA followed by spraying with phages significantly reduced Salmonella from chicken skin by up to 2.5 logs, compared to use of chlorine, low levels of PAA, or phage alone (0.5–1.5 logs). | [59] |
Salmonella spp. | SalmoFresh™ | Treatment of chicken breast fillets by dipping or surface application of a Salmonella-specific bacteriophage preparation and storage at 4 °C significantly reduced Salmonella contamination by up to 0.9 log; further, storing the meat in modified atmospheric packaging after surface application produced a higher reduction in bacterial counts (up to 1.2 logs). | [60] |
Salmonella spp. | SalmoLyse® | A phage cocktail was sprayed onto experimentally contaminated raw pet food ingredients, including chicken, tuna, turkey, cantaloupe, and lettuce, and reduced the levels of the targeted bacteria by ~0.4–1.1 logs. | [61] |
Salmonella spp. | SJ2 | Application of the phage SJ2 significantly reduced Salmonella colonies recovered from experimentally contaminated ground pork and eggs with a larger reduction observed at room temperature, compared to 4 °C. After treatment, Salmonella colonies were screened for phage resistance, and significantly more phage-resistant Salmonella isolates were recovered from eggs, compared with ground pork. | [62] |
Salmonella spp. | PhageGuard S™ (formerly Salmonelex™) | Boneless chicken thighs and legs were experimentally contaminated with Salmonella serovars isolated from ground chicken or other sources. A larger reduction of Salmonella was achieved when the bacteriophage preparation was diluted in tap water, compared to filtered water prior to application, and the phage cocktail was more effective against Salmonella isolated from other sources, compared to those from ground chicken. | [63] |
Salmonella spp. | PhageGuard S™ (formerly Salmonelex™) | Treatment with a bacteriophage cocktail or irradiation significantly reduced (~1 log) the level of Salmonella on experimentally contaminated ground beef trim, and a combination of these methods decreased bacterial contamination by ~2 logs. | [64] |
Shigella spp. | SD-11, SF-A2, SS-92 | Shigella counts were reduced by ~1–4 logs on pieces of spiced chicken after application of a phage cocktail or each of the component phages and storage at 4 °C. | [65] |
Shigella sonnei | ShigaShield™ | Application of a five-phage, Shigella-specific cocktail to various RTE foods, including lettuce, melon, smoked salmon, corned beef and pre-cooked chicken, reduced the recovery of Shigella ~1.0–1.4 logs at the highest phage concentration applied compared to control. | [66] |
Staphylococcus aureus | Φ88, Φ35 | S. aureus levels decreased below the limit of detection in experimentally contaminated whole milk after treatment, with a two-phage cocktail and storage at 37 °C. After phage treatment, S. aureus was not recovered from the acid curd after storage for 4 h at 25 °C, and was eliminated from the renneted curd after 1 h at 30 °C. | [67] |
Staphylococcus aureus | vB_SauS-phi-IPLA35, vB_SauS-phi-SauS-IPLA88 | Counts of S. aureus were significantly decreased in cheese made using milk treated with phages compared to milk without the addition of phages. The microbiota of the cheese was not impacted by the addition of the phages. | [68] |
Company | Phage Product | Target Organism(s) | Regulatory | Certifications | References |
---|---|---|---|---|---|
FINK TEC GmbH (Hamm, Germany) | Secure Shield E1 | E. coli | FDA, GRN 724 pending as of 19 March 2018 | ||
Intralytix, Inc. (Baltimore, MD, USA) | Ecolicide® (EcolicidePX™) | E. coli O157:H7 | USDA, FSIS Directive 7120.1 | ||
EcoShield™ | E. coli O157:H7 | FDA, FCN 1018; Israel Ministry of Health; Health Canada | Kosher; Halal | [17,27,29,30,32,34] | |
ListShield™ | L. monocytogenes | FDA, 21 CFR 172.785; FDA, GRN 528; EPA Reg. No. 74234-1; Israel Ministry of Health; Health Canada | Kosher; Halal; OMRI | [10,35,36] | |
SalmoFresh™ | Salmonella spp. | FDA, GRN 435; USDA, FSIS Directive 7120.1; Israel Ministry of Health; Health Canada | Kosher; Halal; OMRI | [59,60] | |
ShigaShield™ (ShigActive™) | Shigella spp. | FDA, GRN 672 | [66,69] | ||
Micreos Food Safety (Wageningen, Netherlands) | PhageGuard Listex™ | L. monocytogenes | FDA, GRN 198/218; FSANZ; EFSA; Swiss BAG; Israel Ministry of Health; Health Canada | Kosher; Halal; OMRI; SKAL | [37,38,39,40,43,44,45,46,47] |
PhageGuard S™ | Salmonella spp. | FDA, GRN 468; FSANZ; Swiss BAG; Israel Ministry of Health; Health Canada | Kosher; Halal; OMRI; SKAL | [63,64] | |
E. coli O157:H7 | FDA, GRN 757 pending as of 19 March 2018 | ||||
Passport Food Safety Solutions (West Des Moines, IA, USA) | Finalyse® | E. coli O157:H7 | USDA, FSIS Directive 7120.1 | ||
Phagelux (Shanghai, China) | AgriPhage™ | Xanthomonas campestris pv. vesicatoria, Pseudomonas syringae pv. tomato | EPA Reg. No. 67986-1 | ||
SalmoPro® | Salmonella spp. | FDA, GRN 603 | |||
Salmonella spp. | FDA, GRN 752 pending as of March 19, 2018 |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Moye, Z.D.; Woolston, J.; Sulakvelidze, A. Bacteriophage Applications for Food Production and Processing. Viruses 2018, 10, 205. https://doi.org/10.3390/v10040205
Moye ZD, Woolston J, Sulakvelidze A. Bacteriophage Applications for Food Production and Processing. Viruses. 2018; 10(4):205. https://doi.org/10.3390/v10040205
Chicago/Turabian StyleMoye, Zachary D., Joelle Woolston, and Alexander Sulakvelidze. 2018. "Bacteriophage Applications for Food Production and Processing" Viruses 10, no. 4: 205. https://doi.org/10.3390/v10040205
APA StyleMoye, Z. D., Woolston, J., & Sulakvelidze, A. (2018). Bacteriophage Applications for Food Production and Processing. Viruses, 10(4), 205. https://doi.org/10.3390/v10040205