Use of Bacteriophages to Improve Food Safety

Öz

Food safety is a major concern for human health. Foodborne pathogens are responsible for several millions of cases annually worldwide. In order to inactivate these foodborne pathogens, numerous methods are available. However, these conventional methods have several drawbacks, such as heat treatment significantly affects nutritional properties of foods, chemical sanitizers leave residue on foods and food contact surfaces, high-pressure applications require special and relatively expensive equipment, and antibiotic use leads microorganisms to develop antibiotic resistance. One method that could overcome these drawbacks is bacteriophage application. Bacteriophages, or shortly phages, are viruses that infect bacteria, and they are found everywhere where bacteria are found. During the infection progeny phages are produced and phages inactivate bacteria by bursting the cell wall. Phage isolation can easily be done from natural sources like animal feces, wastewater, and sewage. In recent years, there have been many studies about phage application. When phages are applied on foods, they do not affect sensory or nutritional values of foods, humans, and environment. Also, since they are host specific, they only inactivate pathogenic bacteria. In addition, they have a different inactivation mechanism than antibiotics so phages can inactive antibiotic resistant bacteria as well. There are phage-based commercial products that are approved to be used on foods. On the other hand, there are technical and regulatory challenges. To overcome technical challenges, academic studies are being conducted. This study aims to generalize the use of bacteriophages in food industry by reviewing research articles in this area.

Anahtar Kelimeler

• bacteriophages
• phages
• food safety
• foodborne pathogens

Bakteriyofajların Gıda Güvenliğini Artırmak Amacıyla Kullanılması

Öz

Gıda güvenliği insan sağlığı ile önemli derecede ilgilidir. Gıda kaynaklı patojenler dünya çapında yılda milyonlarca vakaya sebep olmaktadırlar. Bu patojenleri inaktive etmek adına sayısız yöntem bulunmaktadır. Fakat bu alışılagelmiş metotların bazı dezavantajları bulunmaktadır. Örneğin ısıl işlemler gıdanın besleyici özelliklerine zarar verirler, kimyasal ilaçlar gıda üzerinde kalıntı bırakırlar, yüksek basınç gibi işlemler yüksek maliyetli cihaz gerektirirler ve antibiyotiklerin kullanımı sonucunda mikroorganizmalar hızla antibiyotik dirençliliği kazanmaktadırlar. Bakteriyofajlar bu sorunların üstesinden gelebilecek bir metot olarak görülmektedir. Bakteriyofajlar, ya da kısaca fajlar, doğada bakterinin bulunduğu her yerde bulunan, hedef mikroorganizmaya özgü ve sadece bakterileri enfekte eden virüslerdir. Enfeksiyon sonucu hücre içinde fajlar çoğalırlar ve bakterinin hücre duvarını patlatarak bakteriyi inaktive ederler. Doğada büyükbaş, küçükbaş ve kümes hayvanlarının dışkıları, atık sular ve kanalizasyonlar gibi bakterilerin yoğun bir şekilde bulunduğu yerlerden rahatça faj izolasyonu yapılabilmektedir. Son yıllarda fajların gıda üzerinde kullanılması ile ilgili birçok çalışma yapılmıştır. Fajlar gıda üzerine uygulandıklarında gıdanın duyusal ve besleyici özelliklerine, insana, çevreye zarar vermezler ve hedef bakteriye özgü olduklarından yararlı mikroorganizmaları inaktive etmezler. Ayrıca inaktivasyon mekanizması antibiyotiklerden farklı olduğundan antibiyotiğe dirençli bakterileri de etkili bir şekilde inaktive ederler. Kimyasal uygulama içermediğinden gıda üzerinde bir kimyasal kalıntı bırakmaz ve uygulanması sırasında pahalı ekipmanlara ihtiyaç duyulmaz. Ticarî olarak gıda üzerinde direkt kullanımı onaylanmış faj bazlı ürünler bulunmaktadır. Öte yandan bakteriyofajların gıda üzerinde kullanılmalarının teknik ve yasal zorlukları da bulunmaktadır. Teknik zorlukları aşmak amacıyla akademik çalışmalar devam etmektedir. Yasal olarak ise bakteriyofaj kullanımı ABD ve Avrupa Birliği’nde belli başlı ürünlerde onay almıştır. Bu çalışma, bu alanda yapılan özgün çalışmaları derleyerek bakteriyofaj kullanımının yaygınlaştırılmasını amaçlamaktadır. 

Anahtar Kelimeler

• bakteriyofaj
• faj
• gıda güvenliği
• gıda kaynaklı patojenler

Kaynakça

1. Havelaar AH, Kirk MD, Torgerson PR, et al. World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Medicine. 2015;12(12):e1001923. doi:10.1371/journal.pmed.1001923.
2. Scharff RL. Economic Burden from Health Losses Due to Foodborne Illness in the United States. Journal of Food Protection. 2012;75(1):123-131. doi:10.4315/0362-028X.JFP-11-058.
3. Moye ZD, Woolston J, Sulakvelidze A. Bacteriophage Applications for Food Production and Processing. Viruses. 2018;10(4). doi:10.3390/v10040205.
4. López-Cuevas O, Medrano-Félix JA, Castro-Del Campo N, Chaidez C. Bacteriophage applications for fresh produce food safety. International Journal of Environmental Health Research. 2021;31(6):687-702. doi:10.1080/09603123.2019.1680819.
5. Hudson JA, Bigwood T, Premaratne A, Billington C, Horn B, McIntyre L. Potential to use ultraviolet-treated bacteriophages to control foodborne pathogens. Foodborne Pathogens and Disease. 2010;7(6):687-693. doi:10.1089/fpd.2009.0453.
6. Food and Drug Administration. Get the Facts about Listeria. https://www.fda.gov/animal-veterinary/animal-health-literacy/get-facts-about-listeria. Published Date 2020. Accessed Date October 3 2021.
7. Perera MN, Abuladze T, Li M, Woolston J, Sulakvelidze A. Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiology. 2015;52:42-48. doi:10.1016/j.fm.2015.06.006.
8. Centers for Disease Control and Prevention. Salmonella and Food. https://www.cdc.gov/foodsafety/communication/salmonella-food.html. Published Date 2021.

9. Huang C, Shi J, Ma W, et al. Isolation, characterization, and application of a novel specific Salmonella bacteriophage in different food matrices. Food Research International. 2018;111:631-641. doi:https://doi.org/10.1016/j.foodres.2018.05.071.
10. Centers for Disease Control and Prevention. Questions and Answers. https://www.cdc.gov/ecoli/general/index.html. Published Date 2014. Accessed Date October 3, 2021.
11. World Health Organization. E. coli. https://www.who.int/news-room/fact-sheets/detail/e-coli. Published Date 2018. Accessed Date October 3, 2021.
12. Tekiner İH, Özpınar H. Occurrence and characteristics of extended spectrum beta-lactamases-producing Enterobacteriaceae from foods of animal origin. Brazilian Journal of Microbiology. 2016;47(2):444-451. doi:https://doi.org/10.1016/j.bjm.2015.11.034.
13. Ferguson S, Roberts C, Handy E, Sharma M. Lytic bacteriophages reduce Escherichia coli O157. Bacteriophage. 2013;3(1):e24323. doi:10.4161/bact.24323.
14. Hudson JA, Billington C, Premaratne A, On SLW. Inactivation of Escherichia coli O157:H7 using ultraviolet light-treated bacteriophages. Food Science and Technology International. 2016;22(1):3-9. doi:10.1177/1082013214560445.
15. Snyder AB, Perry JJ, Yousef AE. Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce. International Journal of Food Microbiology. 2016;236:90-97. doi:10.1016/j.ijfoodmicro.2016.07.023.
16. Aslam A, Okafor CN. Shigella. In: StatPearls; 2021.
17. Shahin K, Bouzari M, Wang R, Yazdi M. Prevalence and molecular characterization of multidrug-resistant Shigella species of food origins and their inactivation by specific lytic bacteriophages. International Journal of Food Microbiology. 2019;305:108252. doi:https://doi.org/10.1016/j.ijfoodmicro.2019.108252.
18. Centers for Disease Control and Prevention. Campylobacter (Campylobacteriosis). https://www.cdc.gov/campylobacter/index.html. Published Date December 23, 2019.
19. Hammerl JA, Jäckel C, Alter T, et al. Reduction of campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PloS One. 2014;9(12):e114785-e114785. doi:10.1371/journal.pone.0114785.
20. Figueiredo ACL, Almeida RCC. Antibacterial efficacy of nisin, bacteriophage P100 and sodium lactate against Listeria monocytogenes in ready-to-eat sliced pork ham. Brazilian Journal of Microbiology . 2017;48(4):724-729. doi:10.1016/j.bjm.2017.02.010.
21. Silva ENG, Figueiredo ACL, Miranda FA, de Castro Almeida RC. Control of Listeria monocytogenes growth in soft cheeses by bacteriophage P100. Brazilian Journal Of Microbiology. 2014;45(1):11-16. doi:10.1590/s1517-83822014000100003
22. Hong Y, Schmidt K, Marks D, et al. Treatment of Salmonella-contaminated eggs and pork with a broad-spectrum, single bacteriophage: assessment of efficacy and resistance development. Foodborne Pathogens and Disease. 2016;13(12):679-688. doi:10.1089/fpd.2016.2172.
23. Yeh Y, de Moura FH, Van Den Broek K, de Mello AS. Effect of ultraviolet light, organic acids, and bacteriophage on Salmonella populations in ground beef. Meat science. 2018;139:44-48. doi:10.1016/j.meatsci.2018.01.007.
24. Islam MS, Hu Y, Mizan MFR, et al. Characterization of salmonella phage LPST153 that effectively targets most prevalent salmonella serovars. Microorganisms. 2020;8(7). doi:10.3390/microorganisms8071089.
25. Li YK, Wu X, Chen H, et al. A bacteriophage JN02 infecting multidrug-resistant Shiga toxin-producing Escherichia coli: isolation, characterisation and application as a biocontrol agent in foods. International Journal of Food Science \& Technology. 2021;n/a(n/a). doi:https://doi.org/10.1111/ijfs.15070.
26. Mangieri N, Picozzi C, Cocuzzi R, Foschino R. Evaluation of a potential bacteriophage cocktail for the control of shiga-toxin producing Escherichia coli in food. Frontiers in Microbiology. 2020;11:1801. doi:10.3389/fmicb.2020.01801.
27. 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(3):e0175256-e0175256. doi:10.1371/journal.pone.0175256.
28. Shahin K, Bouzari M. Bacteriophage application for biocontrolling Shigella flexneri in contaminated foods. Journal of Food Science and Technology. 2018;55(2):550-559. doi:10.1007/s13197-017-2964-2.
29. D’Angelantonio D, Scattolini S, Boni A, et al. Bacteriophage therapy to reduce colonization of campylobacter jejuni in broiler chickens before slaughter. Viruses. 2021;13(8). doi:10.3390/v13081428.
30. Chinivasagam HN, Estella W, Maddock L, et al. Bacteriophages to control campylobacter in commercially farmed broiler chickens, in Australia. Frontiers in Microbiology. 2020;11:632. doi:10.3389/fmicb.2020.00632.
31. Pinto G, Almeida C, Azeredo J. Bacteriophages to control Shiga toxin-producing E. coli – safety and regulatory challenges. Critical Reviews in Biotechnology. 2020;40(8):1081-1097. doi:10.1080/07388551.2020.1805719.
32. Duc HM, Son HM, Yi HPS, et al. Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157:H7 in different food matrices. Food Research International. 2020;131:108977. doi:https://doi.org/10.1016/j.foodres.2020.108977.