Gıda teknolojilerinde inovatif bir yaklaşım olarak “Bakteriyofajlar”

Öz

Gıda üretim zincirinde kontamine olmuş gıdalardaki patojenik mikroorganizmaların antibiyotiklere direnç göstermeye başlaması, Avrupa’da ve ABD’de hayvan beslemede antibiyotik kullanımına yasal sınırlamaların getirilmesi ve bunun yanısıra tüketicilerin de kimyasal kontaminasyon içermeyen ürün talepleri doğrultusunda gıdaların patojenlerden arındırılmasında alternatif kontrol yöntemlerine gereksinim duyulmaktadır. Son yıllarda canlı mikrobiyal hücreleri enfekte eden virüsler olarak tanımlanan fajlar, tarım ve gıda sektöründe farklı amaçlarla ticarileştirilmeye başlanmıştır. Gıdalarda patojenlerin yok edilmesinde genel olarak “çiftlikten sofraya” kadar tüm gıda zinciri aşamalarında uygulanabilmektedir. Bakteriyofajlar, özellikle gıda endüstrisinde ekipman ve temas yüzeylerinin dezenfeksiyonu (biyosanitasyon), kolay bozulabilir gıdalarda doğal koruyucu olarak kullanılarak, ürünün raf ömrünün uzatılması (biyokoruma) ve çiğ süt, et ve taze gıdalarda dekontaminasyon (biyokontrol) amacıyla kullanılabilmektedir. Antibiyotik alternatifi olarak hayvan ve bitki yetiştiriciliğinde terapötik amaçlı kullanılmasının yanı sıra, gıda endüstrisindeki temel problemlerden biri olan biyofilm oluşumunu önleme ve elimine etmede, patojen bakterilerin hızlı tespitinde kullanılması konusunda yoğun araştırmalar devam etmektedir. Bakteriyofaj uygulamaları, Listeria monocytogenes, Escherichia coli O157:H7, Staphylococcus aureus, Pseudomonas spp. ve Salmonella spp. gibi gıda kaynaklı patojenler üzerine yoğunlaşmıştır. Fajın gıda güvenliğiyle ilgili iki benzersiz özelliği arasında, hayvan ile bitki hücrelerine ve doğal mikrobiyotaya zarar vermemeleri sıralanabilmektedir. Fajların konakçılarına özgü özellikleri, sadece sınırlı sayıda bakteri suşunu enfekte edebilmeleri açısından bir dezavantaj olarak değerlendirilmektedir. Buna ek olarak çevresel faktörlerden (ultraviyole (UV) ışınları, sıcaklık ve nem dalgalanmaları, bitki koruması için kullanılan kimyasalların kalıntıları gibi) etkilenebilir olması faj uygulamasında çeşitli zorluklar yaratmaktadır. Bu derlemede, son yıllarda inovatif bir yaklaşım olarak değerlendirilen bakteriyofajların ticarileştirilme süreci, tarım ve gıda alanlarındaki uygulamalarının avantaj ve dezavantajları detaylı olarak incelenerek, hasat öncesi ve hasat sonrası gıda işlemede kullanılabilirliği değerlendirilmektedir.

Anahtar Kelimeler

• Virüs
• Bakteriyofaj
• Faj Terapisi
• Gıda Teknolojisi
• Biyofilm
• Biyoajan

"Bacteriophages" as an Innovative Approach in Food Technologies

Abstract

In line with the resistance of pathogenic microorganisms in contaminated foods to antibiotics in the food production chain, the imposition of legal restrictions on the use of antibiotics in animal nutrition in Europe and the USA, and the demand of consumers for products that do not contain chemical contamination, alternative control methods are required for the decontamination of foods from pathogens. Phages, defined as viruses that infect living microbial cells in recent years, have started to be commercialized for different purposes in the agriculture and food industry. It can generally be applied at all stages of the food chain from "farm to table" in the destruction of pathogens in foods. Bacteriophages, especially in the food industry, can be used for disinfection of equipment and contact surfaces (biosanitation), using as natural preservatives in perishable foods, extending the shelf life of the product (bioprotection), and decontamination (biocontrol) in raw milk, meat, and fresh foods. In addition to its therapeutic use in animal and plant breeding as an alternative to antibiotics, intensive research continues on its use in the prevention and elimination of biofilm formation, one of the main problems in the food industry, and rapid detection of pathogenic bacteria. Bacteriophage applications have focused on foodborne pathogens such as Listeria monocytogenes, Escherichia coli O157: H7, Staphylococcus aureus, Pseudomonas spp. and Salmonella spp. Two unique characteristics of phage regarding food safety are that they do not damage animal and plant cells and do not harm the natural microbiota. The characteristics of phages specific to their hosts are seen as a disadvantage in that they can only infect a limited number of bacterial strains. Besides, being easily affected by environmental factors (such as ultraviolet (UV) rays, temperature, and humidity fluctuations, and chemical agent residues used for plant protection) that creates various difficulties in phage application. In this review, it is aimed at a different perspective by examining the advantages and disadvantages of the applications of bacteriophages in agriculture and food fields, which have been considered as an innovative approach in recent years.

Keywords

• Virus
• Bacteriophage
• Phage Therapy
• Food Technology
• Biofilm
• Bioagent

References

1. Adams, M.H. (1959). Bacteriophages. New York, USA, Interscience Publishers.
2. Adriaenssens, E. M., Van Vaerenbergh, J., Vandenheuvel, D., Dunon, V., Ceyssens, P. J., De Proft, M., ... & Lavigne, R. (2012). T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by ‘Dickeya solani’. PloS one, 7(3), e33227.
3. Aldayel, M. F. (2019). Biocontrol strategies of antibiotic-resistant, highly pathogenic bacteria and fungi with potential bioterrorism risks: Bacteriophage in focus. Journal of King Saud University-Science, 31(4), 1227-1234.
4. Amarillas, L., Lightbourn‐Rojas, L., Angulo‐Gaxiola, A. K., Basilio Heredia, J., González‐Robles, A., & León‐Félix, J. (2018). The antibacterial effect of chitosan‐based edible coating incorporated with a lytic bacteriophage against Escherichia coli O157: H7 on the surface of tomatoes. Journal of Food Safety, 38(6), e12571.
5. Arthur, T. M., Kalchayanand, N., Agga, G. E., Wheeler, T. L., & Koohmaraie, M. (2017). Evaluation of bacteriophage application to cattle in lairage at beef processing plants to reduce Escherichia coli O157: H7 prevalence on hides and carcasses. Foodborne pathogens and disease, 14(1), 17-22.
6. Atamer, Z., Samtlebe, M., Neve, H., Heller, K. J., & Hinrichs, J. (2013). elimination of bacteriophages in whey and whey products. Frontiers in microbiology, 4, 191.
7. Bach, S. J., Johnson, R. P., Stanford, K., & McAllister, T. A. (2009). Bacteriophages reduce Escherichia coli O157: H7 levels in experimentally inoculated sheep. Canadian journal of animal science, 89(2), 285-293.
8. Balogh, B., Canteros, B. I., Stall, R. E., & Jones, J. B. (2008). Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Disease, 92(7), 1048-1052.

9. Balogh, B., Jones, J. B., Momol, M. T., Olson, S. M., Obradovic, A., King, P., & Jackson, L. E. (2003). Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant disease, 87(8), 949-954.
10. Barberis, S., Quiroga, H. G., Barcia, C., Talia, J. M., & Debattista, N. (2018). Natural food preservatives against microorganisms. In Food Safety and Preservation (pp. 621-658). Academic Press.
11. Boulé, J., Sholberg, P. L., Lehman, S. M., O'gorman, D. T., & Svircev, A. M. (2011). Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada. Canadian journal of plant pathology, 33(3), 308-317.
12. Brüssow, H. and Kutter, E. (2005). Phage ecology. In E. Kutter & A. Sulakvelidze, Bacteriophages: biology and applications. Florida: Boca Raton CRC Press. pp: 129-163.
13. Buttimer, C., Hendrix, H., Lucid, A., Neve, H., Noben, J. P., Franz, C., ... & Coffey, A. (2018). Novel N4-Like bacteriophages of Pectobacterium atrosepticum. Pharmaceuticals, 11(2), 45.
14. Carlton RM.(1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp (Warsz) 1999; 47:267-74; PMID: 10604231.
15. Carvalho, C. M., Gannon, B. W., Halfhide, D. E., Santos, S. B., Hayes, C. M., Roe, J. M., & Azeredo, J. (2010). The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC microbiology, 10(1), 232.
16. Casey, A.; Co_ey, A.; McAuli_e, O. (2017). Genetics and genomics of bacteriophages: The evolution of bacteriophage genomes and genomic research. Bacteriophages Biol. Technol. Ther., 1–26.
17. Choińska-Pulit, A., Mituła, P., Śliwka, P., Łaba, W., & Skaradzińska, A. (2015). Bacteriophage encapsulation: Trends and potential applications. Trends in Food Science & Technology, 45(2), 212-221.
18. Coffey, A., & Ross, R. P. (2002). Bacteriophage-resistance systems in dairy starter strains: molecular analysis to application. Antonie van Leeuwenhoek, 82(1-4), 303-321.
19. Cogliani, C., Goossens, H. and Greko, C. (2011). Restricting antimicrobial use in food animals: Lessons from Europe. Microbe. 6: 274-279.
20. Czajkowski, R., Ozymko, Z., Zwirowski, S., & Lojkowska, E. (2014). Complete genome sequence of a broad-host-range lytic Dickeya spp. bacteriophage ϕD5. Archives of virology, 159(11), 3153-3155.
21. Das, M., Bhowmick, T. S., Ahern, S. J., Young, R., & Gonzalez, C. F. (2015). Control of Pierce's disease by phage. PLoS One, 10(6), e0128902.
22. Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nature reviews Drug discovery, 2(2), 114-122.
23. de Melo, A. G., Levesque, S., & Moineau, S. (2018). Phages as friends and enemies in food processing. Current opinion in biotechnology, 49, 185-190.
24. Dogan, B., & Boor, K. J. (2003). Genetic diversity and spoilage potential among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Applied and Environmental Microbiology, 69, 130–138.
25. El-Shibiny, A., & El-Sahhar, S. (2017). Bacteriophages: the possible solution to treat infections caused by pathogenic bacteria. Canadian journal of microbiology, 63(11), 865-879.
26. Endersen, L., O'Mahony, J., Hill, C., Ross, R. P., McAuliffe, O., & Coffey, A. (2014). Phage therapy in the food industry. Annual review of food science and technology, 5, 327-349.
27. Fan, H., & Tong, Y. (2012). Y., Potential Duel-Use of Bacteriophage Related Technologies in Bioterrorism and Biodefense. Journal of bioterrorism and biodefense, 3(121), 4.
28. Faruque, S. M., & Mekalanos, J. J. (2012). Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence, 3(7), 556-565.
29. Fernandez-Cassi, X., Timoneda, N., Martínez-Puchol, S., Rusinol, M., Rodriguez-Manzano, J., Figuerola, N., ... & Girones, R. (2018). Metagenomics for the study of viruses in urban sewage as a tool for public health surveillance. Science of the Total Environment, 618, 870-880.
30. Frampton, R. A., Taylor, C., Moreno, A. V. H., Visnovsky, S. B., Petty, N. K., Pitman, A. R., & Fineran, P. C. (2014). Identification of bacteriophages for biocontrol of the kiwifruit canker phytopathogen Pseudomonas syringae pv. actinidiae. Applied and Environmental Microbiology, 80(7), 2216-2228.
31. Fujiwara, A., Fujisawa, M., Hamasaki, R., Kawasaki, T., Fujie, M., & Yamada, T. (2011). Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Applied and environmental microbiology, 77(12), 4155-4162.
32. Galarce, N., Escobar, B., Rojas, V., Navarro, C., Turra, G., Robeson, J., & Borie, C. (2016). Application of a virulent bacteriophage cocktail leads to reduction of Salmonella enterica serovar Enteritidis counts in processed meat products. Biocontrol Science and Technology, 26(4), 462-475.
33. Garcia, P., Martinez, B., Obeso, J. M., & Rodriguez, A. (2008). Bacteriophages and their application in food safety. Letters in applied microbiology, 47(6), 479-485.
34. Garneau, J. and Moineau, S. (2011) Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb Cell Fact 10, S20.
35. Ghannad, M. S., & Mohammadi, A. (2012). Bacteriophage: time to re-evaluate the potential of phage therapy as a promising agent to control multidrug-resistant bacteria. Iranian journal of basic medical sciences, 15(2), 693.
36. Goodridge, L. D., & Bisha, B. (2011). Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage, 1(3), 130-137.
37. Gouvêa, D. M., Mendonça, R. C. S., Lopez, M. E. S., & Batalha, L. S. (2016). Absorbent food pads containing bacteriophages for potential antimicrobial use in refrigerated food products. LWT-Food Science and Technology, 67, 159-166.
38. Greer, G. G., & Dilts, B. D. (2002). Control of Brochothrix thermosphacta spoilage of pork adipose tissue using bacteriophages. Journal of food protection, 65(5), 861-863.
39. Greer, G.G. (1982) Psychrotrophic bacteriophages for beef spoilage pseudomonads. J Food Prot 45:1318–1325
40. Greer, G.G. (1988) Effects of phage concentration, bacterial density, and temperature on phage control of beef spoilage. J Food Sci 53:1226– 122
41. Gupta R, Prasad Y.(2011). Efficacy of polyvalent bacteriophage p-27/HP to control multidrug resistant Staphylococcus aureus associated with human infections. Curr Microbiol , 62:255-60; PMID: 20607539; DOI: 10.1007/s00284-010-9699-x
42. Hagens, S., & Loessner, M. J. (2007). Application of bacteriophages for detection and control of foodborne pathogens. Applied microbiology and biotechnology, 76(3), 513-519.
43. Halter, M. C., & Zahn, J. A. (2018). Characterization of a novel lytic bacteriophage from an industrial Escherichia coli fermentation process and elimination of virulence using a heterologous CRISPR–Cas9 system. Journal of industrial microbiology & biotechnology, 45(3), 153-163.
44. Hammerl, J. A., Jäckel, C., Alter, T., Janzcyk, P., Stingl, K., Knüver, M. T., & Hertwig, S. (2014). Reduction of Campylobacter jejuni in broiler chicken by successive application of group II and group III phages. PLoS One, 9(12).
45. Heidelberg, J. F., Eisen, J. A., Nelson, W. C., Clayton, R. A., Gwinn, M. L., Dodson, R. J., ... & Gill, S. R. (2000). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature, 406(6795), 477-483.
46. Hendrix, R. W. (2002). Bacteriophages: evolution of the majority. Theoretical population biology, 61(4), 471-480.
47. Hermoso, J. A., García, J. L., & García, P. (2007). Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Current opinion in microbiology, 10(5), 461-472.
48. Hernández, I. (2017). Bacteriophages against Serratia as fish spoilage control technology. Frontiers in microbiology, 8, 449.
49. Huff, W. E., Huff, G. R., Rath, N. C., Balog, J. M., & Donoghue, A. M. (2003). Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection. Poultry science, 82(7), 1108-1112.
50. Hussain, M. A., Liu, H., Wang, Q., Zhong, F., Guo, Q., & Balamurugan, S. (2017). Use of encapsulated bacteriophages to enhance farm to fork food safety. Critical reviews in food science and nutrition, 57(13), 2801-2810.
51. Islam, M., Zhou, Y., Liang, L., Nime, I., Liu, K., Yan, T., ... & Li, J. (2019). Application of a Phage Cocktail for Control of Salmonella in Foods and Reducing Biofilms. Viruses, 11(9), 841.
52. Jones, J. B., Vallad, G. E., Iriarte, F. B., Obradović, A., Wernsing, M. H., Jackson, L. E., ... & Momol, M. T. (2012). Considerations for using bacteriophages for plant disease control. Bacteriophage, 2(4), e23857.
53. Kazi, M., & Annapure, U. S. (2016). Bacteriophage biocontrol of foodborne pathogens. Journal of food science and technology, 53(3), 1355-1362.
54. Kim, J., Kim, M., Kim, S., & Ryu, S. (2017). Sensitive detection of viable Escherichia coli O157: H7 from foods using a luciferase-reporter phage phiV10lux. International journal of food microbiology, 254, 11-17.
55. Kim, M. H., Park, S. W., & Kim, Y. K. (2011). Bacteriophages of Pseudomonas tolaasii for the biological control of brown blotch disease. Journal of the Korean Society for Applied Biological Chemistry, 54(1), 99-104.
56. Kutateladze, M., & Adamia, R. (2010). Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends in biotechnology, 28(12), 591-595.
57. Lang, J. M., Gent, D. H., & Schwartz, H. F. (2007). Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant disease, 91(7), 871-878.
58. Langsrud, S., Sidhu, M. S., Heir, E., & Holck, A. L. (2003). Bacterial disinfectant resistance—a challenge for the food industry. International Biodeterioration & Biodegradation, 51(4), 283-290.
59. Lehman, S.M. (2007). Development of a Bacteriophage-Based Biopesticide for Fire Blight. Ph.D. Thesis, Brock University, St. Catharines, ON, Canada, 2007.
60. Leverentz B, Conway WS, Camp MJ, et al. (2003) Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl Environ Microbiol 69: 4519–4526.
61. Lewis, R., & Hill, C. (2020). Overcoming barriers to phage application in food and feed. Current opinion in biotechnology, 61, 38-44.
62. Lim, J. A., Jee, S., Lee, D. H., Roh, E., Jung, K., Oh, C., & Heu, S. (2013). Biocontrol of Pectobacterium carotovorum subsp. carotovorum using bacteriophage PP1. J Microbiol Biotechnol, 23(8), 1147-1153.
63. Lin, D. M., Koskella, B., & Lin, H. C. (2017). Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World journal of gastrointestinal pharmacology and therapeutics, 8(3), 162.
64. Lorch, A. (1999). Bacteriophages: An alternative to antibiotics. Biotechnology and development monitor, 39, 14-17.
65. Ma, Y., Pacan, J. C., Wang, Q., Xu, Y., Huang, X., Korenevsky, A. and Sabour, P. M. (2008). Microencapsulation of bacteriophage felix O1 into chitosan-alginate microspheres for oral delivery. Appl. Environ. Microbiol. 74: 4799-4805.
66. Marintcheva, B. (2018). Phage therapy, Harnessing the Power of Viruses- Virus-Based Therapeutic Approaches 9.1 https://doi.org/10.1016/B978-0-12-810514-6.00009-X
67. McManus, P. S. (2014). Does a drop in the bucket make a splash? Assessing the impact of antibiotic use on plants. Current opinion in microbiology, 19, 76-82.
68. McManus, P. S., Stockwell, V. O., Sundin, G. W., & Jones, A. L. (2002). Antibiotic use in plant agriculture. Annual review of phytopathology, 40(1), 443-465.
69. Merabishvili, M., Pirnay, J. P., Verbeken, G., Chanishvili, N., Tediashvili, M., Lashkhi, N., ... & Lavigne, R. (2009). Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PloS one, 4(3), e4944.
70. Moineau, S., Tremblay, D., & Labrie, S. (2002). Phages of lactic acid bacteria: from genomics to industrial applications.
71. Monk, A. B., Rees, C. D., Barrow, P., Hagens, S., & Harper, D. R. (2010). Bacteriophage applications: where are we now?. Letters in applied microbiology, 51(4), 363-369.
72. Morozova, V., Kozlova, Y., Shedko, E., Babkin, I., Kurilshikov, A., Bokovaya, O., ... & Ushakova, T. (2018). Isolation and characterization of a group of new Proteus bacteriophages. Archives of virology, 163(8), 2189-2197.
73. Mosteller, T. M., & Bishop, J. R. (1993). Sanitizer efficacy against attached bacteria in a milk biofilm. Journal of food protection, 56(1), 34-41.
74. Naanwaab, C., Yeboah, O. A., Ofori Kyei, F., Sulakvelidze, A., & Goktepe, I. (2014). Evaluation of consumers’ perception and willingness to pay for bacteriophage treated fresh produce. Bacteriophage, 4(4), e979662.
75. Nagy, J. K., Schwarczinger, I., Künstler, A., Pogány, M., & Király, L. (2015). Penetration and translocation of Erwinia amylovora-specific bacteriophages in apple-a possibility of enhanced control of fire blight. European journal of plant pathology, 142(4), 815-827.
76. Nigam, A., Gupta, D., & Sharma, A. (2014). Treatment of infectious disease: beyond antibiotics. Microbiological research, 169(9-10), 643-651.
77. Oliveira, J., Castilho, F., Cunha, A., & Pereira, M. J. (2012). Bacteriophage therapy as a bacterial control strategy in aquaculture. Aquaculture International, 20(5), 879-910.
78. Pereira, C., Silva, Y. J., Santos, A. L., Cunha, ., Gomes, N., & Almeida, A. (2011). Bacteriophages with potential for inactivation of fish pathogenic bacteria: survival, host specificity and effect on bacterial community structure. Marine drugs, 9(11), 2236-2255.
79. Pirnay, J. P., Merabishvili, M., Van Raemdonck, H., De Vos, D., & Verbeken, G. (2018). Bacteriophage production in compliance with regulatory requirements. In Bacteriophagetherapy (pp. 233-252). Humana Press, New York, NY.
80. Połaska, M., & Sokołowska, B. (2019). Bacteriophages—a new hope or a huge problem in the food industry. AIMS microbiology, 5(4), 324.
81. Pujato, S. A., Quiberoni, A., & Mercanti, D. J. (2019). Bacteriophages on dairy foods. Journal of applied microbiology, 126(1), 14-30.
82. Ramirez, K., Cazarez-Montoya, C., LopezMoreno, H. S., Castro-del Campo, N. (2018). Bacteriophage cocktail for biocontrol of Escherichia coli O157:H7: Stability and potential allergenicity study. PLoS ONE, 13(5): 1-19, doi: 10.1371/journal.pone.0195023.
83. Ranjani, P., Gowthami, Y., Gnanamanickam, S. S., & Palani, P. (2018). Bacteriophages: A new weapon for the control of bacterial blight disease in rice caused by Xanthomonas oryzae. Microbiol Biotechnol Lett, 46(4), 346-59.
84. Rao, B. M., & Lalitha, K. V. (2015). Bacteriophages for aquaculture: are they beneficial or inimical. Aquaculture, 437, 146-154.
85. Robinson, R. K. (2014). Encyclopedia of food microbiology. Academic press.
86. Rombouts, S., Volckaert, A., Venneman, S., Declercq, B., Vandenheuvel, D., Allonsius, C. N., ... & Klumpp, J. (2016). Characterization of novel bacteriophages for biocontrol of bacterial blight in leek caused by Pseudomonas syringae pv. porri. Frontiers in microbiology, 7, 279.
87. Rossi, L. P., Almeida, R. C., Lopes, L. S., Figueiredo, A. C., Ramos, M. P., & Almeida, P. F. (2011). Occurrence of Listeria spp. in Brazilian fresh sausage and control of Listeria monocytogenes using bacteriophage P100. Food Control, 22(6), 954-958.
88. Ryan, E.M., Gorman, S.P., Donnelly, R.F., and Gilmore, B.F. (2011). Recent advances in bacteriophage therapy: how delivery routes, formulation, concentration and timing influence the success of phage therapy. J. Pharm. Pharmacol. 63: 1253– 1264. doi:10.1111/j.2042-7158.2011.01324.x. PMID:21899540.
89. Samtlebe, M., Ergin, F., Wagner, N., Neve, H., Küçükçetin, A., Franz, C. M., ... & Atamer, Z. (2016). Carrier systems for bacteriophages to supplement food systems: Encapsulation and controlled release to modulate the human gut microbiota. LWT-Food Science and Technology, 68, 334-340.
90. Shafiani, S., & Malik, A. (2003). Tolerance of pesticides and antibiotic resistance in bacteria isolated from wastewater-irrigated soil. World Journal of Microbiology and Biotechnology, 19(9), 897-901.
91. Shahin, K., Bouzari, M., Wang, R., & Yazdi, M. (2019). Prevalence and molecular characterization of multidrug-resistant Shigella species of food origins and their inactivation by specific lytic bacteriophages. International journal of food microbiology, 305, 108252.
92. Shkoporov, A. N., Khokhlova, E. V., Fitzgerald, C. B., Stockdale, S. R., Draper, L. A., Ross, R. P., & Hill, C. (2018). ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nature communications, 9(1), 1-8.
93. Sillankorva, S. M., Oliveira, H., & Azeredo, J. (2012). Bacteriophages and their role in food safety. International journal of microbiology, 2012.
94. Sillankorva, S., Oliveira, R., Vieira, M. J., Sutherland, I., & Azeredo, J. (2004). Bacteriophage Φ S1 infection of Pseudomonas fluorescens planktonic cells versus biofilms. Biofouling, 20(3), 133-138.
95. Singh, V. P. (2018). Recent approaches in food bio-preservation-a review. Open veterinary journal, 8(1), 104-111.
96. Skurnik, M., Pajunen, M., Kiljunen, S. (2007). Biotechnological challenges of phage therapy. Biotechnol Lett , 29:995-1003; PMID: 17364214; DOI: 10.1007/ s10529-007-9346-1.
97. Slopek, S., Weber-Dabrowska, B., Dabrowski, M., Kucharewicz-Krukowska, A. (1987). Results of bacteriophage treatment of suppurative bacterial infections in the years 1981–1986. Arch. Immunol. Ther. Exp. (Warsz.) 35:569–83
98. Snyder, A. B., Perry, J. J., & Yousef, A. E. (2016). Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce. International journal of food microbiology, 236, 90-97.
99. Strydom, A., & Witthuhn, C. R. (2015). Listeria monocytogenes: a target for bacteriophage biocontrol. Comprehensive Reviews in Food Science and Food Safety, 14(6), 694-704.
100. Sukumaran, A. T., Nannapaneni, R., Kiess, A., & Sharma, C. S. (2016). Reduction of Salmonella on chicken breast fillets stored under aerobic or modified atmosphere packaging by the application of lytic bacteriophage preparation SalmoFreshTM. Poultry Science, 95(3), 668-675.
101. Sulakvelidze, A., Alavidze, Z., & Morris Jr, J. G. (2001). Bacteriophage therapy, Antimicrob. Agents.
102. Sultan, K. S., Ali, T. A., Fahmy, N. A., & El‐Shibiny, A. (2019). Using millimeter‐waves for rapid detection of pathogenic bacteria in food based on bacteriophage. Engineering Reports, 1(1), e12026.
103. Susianto, G., Farid, M. M., Dhany, N. R., & Addy, H. S. (2014). Host range for bacteriophages that infect bacterial blight pathogen on soybean. Procedia Environmental Sciences, 20, 760-766.
104. Svircev, A., Roach, D., & Castle, A. (2018). Framing the Future with Bacteriophages in Agriculture. Viruses, 10(5), 218. doi:10.3390/v10050218
105. Taj, M. K., Ling, J. X., Bing, L. L., Qi, Z., Taj, I., Hassani, T. M., ... & Yunlin, W. (2014). Effect of dilution, temperature and pH on the lysis activity of T4 phage against E. coli bl21. J. Anim. Plant Sci, 24(4), 1252-1255.
106. Thung, T. Y., Premarathne, J. M. K. J. K., San Chang, W., Loo, Y. Y., Chin, Y. Z., Kuan, C. H., ... & Radu, S. (2017). Use of a lytic bacteriophage to control Salmonella Enteritidis in retail food. LWT, 78, 222-225.
107. Tomat, D., Casabonne, C., Aquili, V., Balagué, C., & Quiberoni, A. (2018). Evaluation of a novel cocktail of six lytic bacteriophages against Shiga toxin-producing Escherichia coli in broth, milk and meat. Food microbiology, 76, 434-442.
108. US Environ. Prot. Agency. (2005). Xanthomonas campestris pv. vesicatoria and Pseudomonas syringae pv. tomato specific bacteriophages; exemption from the requirement of a tolerance. Fed. Regist., 70, 16700-4.
109. USFDA. (2006). Food additives permitted for direct addition to food for human consumption; bacteriophage preparation. FDA, Washington, DC. http://www.fda.gov/OHRMS/DOCKETS/98fr/cf0559.pdf. (accessed on 13 January 2015)
110. van Regenmortel, M. H., & Mahy, B. W. (Eds.). (2010). Desk encyclopedia of general virology. Academic Press.
111. van Zyl, L. J., Abrahams, Y., Stander, E. A., Kirby-McCollough, B., Jourdain, R., Clavaud, C., ... & Trindade, M. (2018). Novel phages of healthy skin metaviromes from South Africa. Scientific reports, 8(1), 1-13.
112. Viazis, S., Akhtar, M., Feirtag, J., et al. (2011). Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol 28: 149–157.
113. Vonasek, E. L., Choi, A. H., Sanchez Jr, J., & Nitin, N. (2018). Incorporating phage therapy into WPI dip coatings for applications on fresh whole and cut fruit and vegetable surfaces. Journal of food science, 83(7), 1871-1879.
114. Waldor, M. K., & Mekalanos, J. J. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science, 272(5270), 1910-1914.
115. Wall, S. K., Zhang, J., Rostagno, M. H., & Ebner, P. D. (2010). Phage therapy to reduce preprocessing Salmonella infections in market-weight swine. Appl. Environ. Microbiol., 76(1), 48-53.
116. Wang, Q. and Sabour, P. M. (2010). Encapsulation and controlled release of bacteriophages for food animal production, p. 237-255. In: P. M. Sabour and M. W. Griffiths (eds.), Bacteriophages in the Control of Food- and Waterborne Pathogens. Washington, DC:ASM Press.
117. Wirtanen, G., Saarela, M. A. R. I. A., & Mattila-Sandholm, T. I. I. N. A. (2000). Biofilms–Impact on hygiene in food industries. Biofilms II:Process analysis and applications, 327-372.
118. Zaman, G., Smetsers, A., Kaan, A., Schoenmakers, J., & Konings, R. (1991). Regulation of expression of the genome of bacteriophage M13. Gene V protein regulated translation of the mRNAs encoded by genes I, III, V and X. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1089(2), 183-192.