LYTIC BACTERIOPHAGES EFFECTIVE AGAINST ESCHERICHIA COLI O157:H7, A FOODBORNE PATHOGEN
Year 2020,
Volume: 45 Issue: 4, 635 - 645, 21.06.2020
Tuba Sakin Şahin
,
Nida Urgancı
,
Zeliha Yıldırım
Abstract
Bacteriophages are considered as alternative antibacterial agents in the food industry and phage therapy due to the widespread of multidrug-resistant pathogen bacteria. The objective of this study was to isolate lytic bacteriophages target to foodborne pathogen Escherichia coli O157:H7. For screening of bacteriophages, 51 samples were collected from sewage, wastewaters of fish farms, slaughterhouses and food factories, and 18 bacteriophages were isolated. The titer of the purified phages samples were changed among 1.7×104-1.02×108 PFU/ml. All of the isolated phages had lytic activity against E. coli O157:H7 strains and thus formed clear plaques. Four of 18 phages were found to have inhibitory effects against other E. coli strains including CFAI, ATCC 25922 and DSα in addition to E. coli O157:H7. It was observed that only two phages were infective against Salmonella Kentucky DMC35. The Eco-OH-phages were highly infection ability with EOP values from 0.5 to 0.1 against E. coli O157:H7 strains.
Supporting Institution
the Scientific Research Projects Coordination Unit of Niğde Ömer Halisdemir University
Project Number
GTB 2018/801-BAGEP
References
- Abedon, S.T. (2011). Lysis from without. Bacteriophage 1, 46-49. doi:10.4161/bact.1.1.13980
- Abedon, S.T., Kuhl, S.J., Blasdel, B.G., Kutter, E.M. (2011). Phage treatment of human infections. Bacteriophage, 1:2, 66-85, DOI: 10.4161/ bact.1.2.15845
- Abuladze T., Li M., Menetrez M.Y., Dean T., Senecal A., Sulakvelidze A. (2008). Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microbiol. (74): 6230–6238.
- Adams MH. (1959). Bacteriophages, Interscience Publishers, Inc. New York,.
- Bach SJ, McAllister TA, Veira DM, Gannon VPJ, Holley RA. 2003. Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Animal Research, 52: 89–101.
- Callaway, T.R., Edrington, T.S., Brabban, A.D., Keen, J.E., Anderson, R.C., Rossman, M.L., Engler, M.J., Genovese, K.J., Gwartney, B.L., Reagan, J.O., Poole, T.L., Harvey, R.B., Kutter, E.M., Nisbet, DJ. (2006). Fecal prevalence of Escherichia coli O157, Salmonella, Listeria, and bacteriophage infecting E. coli O157:H7 in feedlot cattle in the southern plains region of the United States. Foodborne Pathog. Dis. 3: 234–244.
- CDC (Centers for Disease Control and Prevention) (2019) Reports of E. coli Outbreak Investigations from 2019. https://www.cdc.gov/ecoli/2018/o157h7-11-18/index.html
- Clokie, M.R.J., Millard, A.D., Letarov, A.V., Heaphy, S. (2011). Phages in nature. Bacteriophage 1:1, 31-45, DOI: 10.4161/bact.1.1.1494231-45
- d’Herelle, F. (1919). Sur le role du microbe bacteriophage dans la typhose aviare. Comptesrendus Acadamy of Science Paris, 169: 932–934.
- Estrada-Garcia, T., Hodges, K., Hecht, G.A., Tarr, P.I. (2013). Escherichia coli. Chapter 8 In: Foodborne Infections and Intoxications. Eds. J. Glenn Morris, Jr. And Morris E. Potter, pp.129 164. Elsevier Inc. CA, USA.
- Hudson J.A., Billington C., Wilson T., On S.L. (2013). Effect of phage and host concentration on the inactivation of Escherichia coli O157:H7 on cooked and raw beef. Food Sci. Technol. Int. 21:104–109.
- Hyman, P., Abedon, S.T. (2010). Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol.70: 217-248. doi: 10.1016/S0065-2164(10)70007-1
- Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan T., Ishii, S. (2017). Environmental Escherichia coli: ecology and public health implications—a review. J. Appl. Microbiol. 123: 570-581.
- Khan, M.M., Nilsson, A.S. (2015). Isolation of phages for phage therapy: a comparison of spot tests and efficiency of plating analyses for determination of host range and efficacy. PLoS One 10:e0118557. doi: 10.1371/journal.pone.0118557
- Letarov, A.V., Kulikov, E.E. (2017). Adsorption of bacteriophages on bacterial cells. Biochemistry (Mosc). 82: 1632‐1658.
- Liao, Y.T., Salvador, A., Harden, L.A., Liu, F., Lavenburg, V.M., Li, R.W., Wu, V.C.H. (2019). Characterization of a lytic bacteriophage as an antimicrobial agent for biocontrol of shiga toxin-producing Escherichia coli O145 strains. Antibiotics 8:74 doi:10.3390/antibiotics8020074
- Lim, J.Y., Yoon, J. W., Hovde, C.J. (2010). A brief overview of Escherichia coli O157:H7 and its plasmid O157. J. Microbiol. Biotechnol. 20(1): 5–14.
- Litt, P.K., Jaroni, D. (2017) Isolation and physio-morphological characterization of Escherichia coli O157:H7-infecting bacteriophages recovered from beef cattle operations. Int. J. Microbiol. 2017: 7013236.
- Lu, Z., Breidt, F. (2015). Escherichia coli O157:H7 bacteriophage Φ241 isolated from an industrial cucumber fermentation at high acidity and salinity. Front. Microbiol. 6:67.
- Mahony, J., McAuliffe, O., Ross, R.P., Sinderen D. (2011). Bacteriophages as biocontrol agents of food pathogens. Curr. Opin. Biotech. 22(2):157-163.
- McLaughlin, M.R., Balaa, M.F., Sims, J., King, R. (2006). Isolation of Salmonella bacteriophages from swine effluent lagoons. J. Environ. Qual. 35: 522-528.
- Meng, J., Zhao, S., Doyle, M.P., Joseph, S.W. (1998). Antibiotic resistance of Escherichia coli O157:H7 and O157:NM isolated from animals, food, and humans. J. Food Prot. 61:1511-1514.
- Mirzaei, M.K., Nilsson, A.S. (2015). Isolation of phages for phage therapy: A comparison of spot tests and efficiency of plating analyses for determination of host range and efficacy. PLoS One 10(3): e0118557. doi:10.1371/journal.pone.0118557
- Niu, Y., McAllister, T., Xu, Y., Johnson, R.P., Stephens, T.P., Stanford, K. (2009). Prevalence and impact of bacteriophages on the presence of Escherichia coli O157:H7 in feedlot cattle and their environment. Appl. Environ. Microbiol. 75: 1271–1278.
- O’Flynn, G., Ross, R. P., Fitzgerald, G. F., Coffey, A. (2004). Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 70(6): 3417–3424.
- Oot, R., Raya, R., Callaway, T., Edrington, T.S., Kutter, E.M., Brabban, A.D. (2007). Prevalence of Escherichia coli O157 and O157: H7-infecting bacteriophages in feedlot cattle feces. Lett. Appl. Microbiol. 45: 445–453.
- Raya, R.R., Varey, P., Oot, R.A., Dyen, M.R., Callaway, T.R., Edrington, T.S., Kutter, E.M., Brabban, A.D. (2006). Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Appl. Environ. Microbiol. 72(9): 6405–6410.
- Raya, R.R., Oot, R.A., Moore-Maley, B., Wieland, S., Callaway, T.R., et al. (2011). Naturally resident and exogenously applied T4-like and T5-like bacteriophages can reduce Escherichia coli O157:H7 levels in sheep guts. Bacteriophage, 1:15–24.
- Ross, A., Ward, S., Hyman, P. (2016). More is better: selecting for broad host range bacteriophages. Front. Microbiol. 7:1352.
- Sarhan W.A., Azzazy, H.M.E. (2015). Phage approved in food, why not as a therapeutic? Expert Rev. Anti Infect. Ther. 13(1): 91–101.
- Schmidt, H., von Maldeghem, J. Frosch, M., Karch, H. (1998). Antibiotic susceptibilities of verocytotoxin-producing Escherichia coli O157 and nonO157 strains isolated from patients and healthy subjects in Germany during 1996. J. Antimicrob. Chemother. 42: 548–550.
- Sharma, M., Patel, J. R., Conway, W. S., Ferguson, S., Sulakvelidze, A. (2009). Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettuce. J. Food Prot. 72(7): 1481–1485.
- Sheng, H., Knecht, H.J., Kudva, I.T., Hovde, C.J. (2006). Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl. Environ. Microbiol. 72: 5359–5366.
- Synnott, A.J., Kuang, Y., Kurimoto, M., Yamamichi, K., Iwano, H., Tanji, Y. (2009). Isolation from sewage influent and characterization of novel Staphylococcus aureus bacteriophages with wide host ranges and potent lytic capabilities. Appl. Environ. Microbiol. 75: 4483–4490.
- Tanji, Y., Shimada, T., Fukudomi, H., Miyanaga, K., Nakai, Y, Unno, H. (2005). Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J. Biosci. Bioengin. 100(3): 280–287.
- Tomat, D., Migliore, L., Aquili, V., Quiberoni, A., Balague, C. (2013). Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli in meat products. Front. Cell. Infect. Microbiol. 3:20. doi.10.3389/fcimb.2013.00020.
- Topka, G., Bloch, S., Nejman-Falenczyk, B., Gasior, T., Jurczak-Kurek, A., Necel, A., Dydecka, A., Richert, M., Wegrzyn, G., Wegrzyn, A. (2019). Characterization of bacteriophage vB-EcoS-95, isolated from urban sewage and revealing extremely rapid lytic development. Front. Microbiol. 9:3326.
- Viazis, S., Akhtar, M., Feirtag, J., Diez-Gonzalez, F. (2011a). 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.
- Viazis, S., Akhtar, M., Feirtag, J., Brabban, A.D., Diez-Gonzalez, F. (2011b). Isolation and characterization of lytic bacteriophages against enterohaemorrhagic Escherichia coli. J. Appl. Microbiol. 110: 1323–1331.
- Xu, J., Chen, M., He, L., Zhang, S., Ding, T., Yao, H., et al. (2016). Isolation and characterization of a T4-like phage with a relatively wide host range within Escherichia coli. J. Basic Microbiol. 56:405–421. doi: 10.1002/jobm.201500440
- Xu, Y., Xinyan Yu, X., Gu, Y., Huang, X., Liu, G., Xiaoqiu Liu, X. (2019). Characterization and genomic study of phage vB_EcoS-B2 infecting multidrug-resistant Escherichia coli. Front. Microbiol. 9:793. doi: 10.3389/fmicb.2018.00793
- Yıldırım Z, Sakin, T, Çoban F. (2018). Isolation of Anti-Escherichia coli O157:H7 bacteriophages and determination of their host ranges. Turkish J. Agri. Food Sci. Technol. 6: 1200-1208.
- Yildirim Z, Sakin T, Çoban F. (2018). Isolation of lytic bacteriophages infecting Salmonella Typhimurium and Salmonella Enteritidis. Acta Biol. Hung. 69: 350–69.
- Yu, P., Mathieu, J., Li, M., Dai, Z., Alvarez, P.J. (2016). Isolation of polyvalent bacteriophages by sequential multiple-host approaches. Appl. Environ. Microbiol. 82: 808–815.
- Zhao, S., White, D.G., Ge, B., Ayers, S., Friedman, S., English, L., Wagner, D., Gaines, S., Meng, J. (2001). Identification and characterization of integron-mediated antibiotic resistance among shiga toxin-producing Escherichia coli isolates. Appl. Environ. Microbiol. 67: 1558–1564.
GIDA KAYNAKLI PATOJEN ESCHERICHIA COLI O157:H7’YE KARŞI ETKİLİ BAKTERİYOFAJLAR
Year 2020,
Volume: 45 Issue: 4, 635 - 645, 21.06.2020
Tuba Sakin Şahin
,
Nida Urgancı
,
Zeliha Yıldırım
Abstract
Bakteriyofajlar, çoklu ilaç dirençli patojen bakterilerin yaygın olması nedeniyle gıda endüstrisinde ve faj terapisinde alternatif antibakteriyel ajanlar olarak kabul edilmektedirler. Bu çalışmanın amacı, gıda kaynaklı patojen Escherichia coli O157:H7'ye etkili litik bakteriyofajları izole etmektir. Bakteriyofajların taranması için kanalizasyon, balık çiftliklerinin, kesimhanelerin ve gıda fabrikalarının atık sularından toplam 51 örnek toplanmış ve 18 bakteriyofaj izole edilmiştir. Saflaştırılmış faj örneklerin titreleri 1.7×104-1.02×108 PFU/ml arasında değişmiştir. İzole edilen fajların tümü, E. coli O157: H7 suşlarına karşı litik aktiviteye sahip olduğu ve bu nedenle berrak plaklar oluşturduğu gözlenmiştir. On sekiz fajdan dördünün, E. coli O157:H7'ye ek olarak CFAI, ATCC 25922 ve DSa dâhil olmak üzere diğer E. coli suşlarına karşı enfektif oldukları bulunmuştur. Sadece iki fajın Salmonella Kentucky DMC35'e karşı enfektif olduğu gözlenmiştir. Eco-OH-fajları, E. coli O157:H7 suşlarına karşı 0.5 ila 0.1 arasında EOP değerleri ile yüksek enfeksiyon kabiliyetine sahip olduğu bulunmuştur.
Project Number
GTB 2018/801-BAGEP
References
- Abedon, S.T. (2011). Lysis from without. Bacteriophage 1, 46-49. doi:10.4161/bact.1.1.13980
- Abedon, S.T., Kuhl, S.J., Blasdel, B.G., Kutter, E.M. (2011). Phage treatment of human infections. Bacteriophage, 1:2, 66-85, DOI: 10.4161/ bact.1.2.15845
- Abuladze T., Li M., Menetrez M.Y., Dean T., Senecal A., Sulakvelidze A. (2008). Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microbiol. (74): 6230–6238.
- Adams MH. (1959). Bacteriophages, Interscience Publishers, Inc. New York,.
- Bach SJ, McAllister TA, Veira DM, Gannon VPJ, Holley RA. 2003. Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Animal Research, 52: 89–101.
- Callaway, T.R., Edrington, T.S., Brabban, A.D., Keen, J.E., Anderson, R.C., Rossman, M.L., Engler, M.J., Genovese, K.J., Gwartney, B.L., Reagan, J.O., Poole, T.L., Harvey, R.B., Kutter, E.M., Nisbet, DJ. (2006). Fecal prevalence of Escherichia coli O157, Salmonella, Listeria, and bacteriophage infecting E. coli O157:H7 in feedlot cattle in the southern plains region of the United States. Foodborne Pathog. Dis. 3: 234–244.
- CDC (Centers for Disease Control and Prevention) (2019) Reports of E. coli Outbreak Investigations from 2019. https://www.cdc.gov/ecoli/2018/o157h7-11-18/index.html
- Clokie, M.R.J., Millard, A.D., Letarov, A.V., Heaphy, S. (2011). Phages in nature. Bacteriophage 1:1, 31-45, DOI: 10.4161/bact.1.1.1494231-45
- d’Herelle, F. (1919). Sur le role du microbe bacteriophage dans la typhose aviare. Comptesrendus Acadamy of Science Paris, 169: 932–934.
- Estrada-Garcia, T., Hodges, K., Hecht, G.A., Tarr, P.I. (2013). Escherichia coli. Chapter 8 In: Foodborne Infections and Intoxications. Eds. J. Glenn Morris, Jr. And Morris E. Potter, pp.129 164. Elsevier Inc. CA, USA.
- Hudson J.A., Billington C., Wilson T., On S.L. (2013). Effect of phage and host concentration on the inactivation of Escherichia coli O157:H7 on cooked and raw beef. Food Sci. Technol. Int. 21:104–109.
- Hyman, P., Abedon, S.T. (2010). Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol.70: 217-248. doi: 10.1016/S0065-2164(10)70007-1
- Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan T., Ishii, S. (2017). Environmental Escherichia coli: ecology and public health implications—a review. J. Appl. Microbiol. 123: 570-581.
- Khan, M.M., Nilsson, A.S. (2015). Isolation of phages for phage therapy: a comparison of spot tests and efficiency of plating analyses for determination of host range and efficacy. PLoS One 10:e0118557. doi: 10.1371/journal.pone.0118557
- Letarov, A.V., Kulikov, E.E. (2017). Adsorption of bacteriophages on bacterial cells. Biochemistry (Mosc). 82: 1632‐1658.
- Liao, Y.T., Salvador, A., Harden, L.A., Liu, F., Lavenburg, V.M., Li, R.W., Wu, V.C.H. (2019). Characterization of a lytic bacteriophage as an antimicrobial agent for biocontrol of shiga toxin-producing Escherichia coli O145 strains. Antibiotics 8:74 doi:10.3390/antibiotics8020074
- Lim, J.Y., Yoon, J. W., Hovde, C.J. (2010). A brief overview of Escherichia coli O157:H7 and its plasmid O157. J. Microbiol. Biotechnol. 20(1): 5–14.
- Litt, P.K., Jaroni, D. (2017) Isolation and physio-morphological characterization of Escherichia coli O157:H7-infecting bacteriophages recovered from beef cattle operations. Int. J. Microbiol. 2017: 7013236.
- Lu, Z., Breidt, F. (2015). Escherichia coli O157:H7 bacteriophage Φ241 isolated from an industrial cucumber fermentation at high acidity and salinity. Front. Microbiol. 6:67.
- Mahony, J., McAuliffe, O., Ross, R.P., Sinderen D. (2011). Bacteriophages as biocontrol agents of food pathogens. Curr. Opin. Biotech. 22(2):157-163.
- McLaughlin, M.R., Balaa, M.F., Sims, J., King, R. (2006). Isolation of Salmonella bacteriophages from swine effluent lagoons. J. Environ. Qual. 35: 522-528.
- Meng, J., Zhao, S., Doyle, M.P., Joseph, S.W. (1998). Antibiotic resistance of Escherichia coli O157:H7 and O157:NM isolated from animals, food, and humans. J. Food Prot. 61:1511-1514.
- Mirzaei, M.K., Nilsson, A.S. (2015). Isolation of phages for phage therapy: A comparison of spot tests and efficiency of plating analyses for determination of host range and efficacy. PLoS One 10(3): e0118557. doi:10.1371/journal.pone.0118557
- Niu, Y., McAllister, T., Xu, Y., Johnson, R.P., Stephens, T.P., Stanford, K. (2009). Prevalence and impact of bacteriophages on the presence of Escherichia coli O157:H7 in feedlot cattle and their environment. Appl. Environ. Microbiol. 75: 1271–1278.
- O’Flynn, G., Ross, R. P., Fitzgerald, G. F., Coffey, A. (2004). Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 70(6): 3417–3424.
- Oot, R., Raya, R., Callaway, T., Edrington, T.S., Kutter, E.M., Brabban, A.D. (2007). Prevalence of Escherichia coli O157 and O157: H7-infecting bacteriophages in feedlot cattle feces. Lett. Appl. Microbiol. 45: 445–453.
- Raya, R.R., Varey, P., Oot, R.A., Dyen, M.R., Callaway, T.R., Edrington, T.S., Kutter, E.M., Brabban, A.D. (2006). Isolation and characterization of a new T-even bacteriophage, CEV1, and determination of its potential to reduce Escherichia coli O157:H7 levels in sheep. Appl. Environ. Microbiol. 72(9): 6405–6410.
- Raya, R.R., Oot, R.A., Moore-Maley, B., Wieland, S., Callaway, T.R., et al. (2011). Naturally resident and exogenously applied T4-like and T5-like bacteriophages can reduce Escherichia coli O157:H7 levels in sheep guts. Bacteriophage, 1:15–24.
- Ross, A., Ward, S., Hyman, P. (2016). More is better: selecting for broad host range bacteriophages. Front. Microbiol. 7:1352.
- Sarhan W.A., Azzazy, H.M.E. (2015). Phage approved in food, why not as a therapeutic? Expert Rev. Anti Infect. Ther. 13(1): 91–101.
- Schmidt, H., von Maldeghem, J. Frosch, M., Karch, H. (1998). Antibiotic susceptibilities of verocytotoxin-producing Escherichia coli O157 and nonO157 strains isolated from patients and healthy subjects in Germany during 1996. J. Antimicrob. Chemother. 42: 548–550.
- Sharma, M., Patel, J. R., Conway, W. S., Ferguson, S., Sulakvelidze, A. (2009). Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettuce. J. Food Prot. 72(7): 1481–1485.
- Sheng, H., Knecht, H.J., Kudva, I.T., Hovde, C.J. (2006). Application of bacteriophages to control intestinal Escherichia coli O157:H7 levels in ruminants. Appl. Environ. Microbiol. 72: 5359–5366.
- Synnott, A.J., Kuang, Y., Kurimoto, M., Yamamichi, K., Iwano, H., Tanji, Y. (2009). Isolation from sewage influent and characterization of novel Staphylococcus aureus bacteriophages with wide host ranges and potent lytic capabilities. Appl. Environ. Microbiol. 75: 4483–4490.
- Tanji, Y., Shimada, T., Fukudomi, H., Miyanaga, K., Nakai, Y, Unno, H. (2005). Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J. Biosci. Bioengin. 100(3): 280–287.
- Tomat, D., Migliore, L., Aquili, V., Quiberoni, A., Balague, C. (2013). Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli in meat products. Front. Cell. Infect. Microbiol. 3:20. doi.10.3389/fcimb.2013.00020.
- Topka, G., Bloch, S., Nejman-Falenczyk, B., Gasior, T., Jurczak-Kurek, A., Necel, A., Dydecka, A., Richert, M., Wegrzyn, G., Wegrzyn, A. (2019). Characterization of bacteriophage vB-EcoS-95, isolated from urban sewage and revealing extremely rapid lytic development. Front. Microbiol. 9:3326.
- Viazis, S., Akhtar, M., Feirtag, J., Diez-Gonzalez, F. (2011a). 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.
- Viazis, S., Akhtar, M., Feirtag, J., Brabban, A.D., Diez-Gonzalez, F. (2011b). Isolation and characterization of lytic bacteriophages against enterohaemorrhagic Escherichia coli. J. Appl. Microbiol. 110: 1323–1331.
- Xu, J., Chen, M., He, L., Zhang, S., Ding, T., Yao, H., et al. (2016). Isolation and characterization of a T4-like phage with a relatively wide host range within Escherichia coli. J. Basic Microbiol. 56:405–421. doi: 10.1002/jobm.201500440
- Xu, Y., Xinyan Yu, X., Gu, Y., Huang, X., Liu, G., Xiaoqiu Liu, X. (2019). Characterization and genomic study of phage vB_EcoS-B2 infecting multidrug-resistant Escherichia coli. Front. Microbiol. 9:793. doi: 10.3389/fmicb.2018.00793
- Yıldırım Z, Sakin, T, Çoban F. (2018). Isolation of Anti-Escherichia coli O157:H7 bacteriophages and determination of their host ranges. Turkish J. Agri. Food Sci. Technol. 6: 1200-1208.
- Yildirim Z, Sakin T, Çoban F. (2018). Isolation of lytic bacteriophages infecting Salmonella Typhimurium and Salmonella Enteritidis. Acta Biol. Hung. 69: 350–69.
- Yu, P., Mathieu, J., Li, M., Dai, Z., Alvarez, P.J. (2016). Isolation of polyvalent bacteriophages by sequential multiple-host approaches. Appl. Environ. Microbiol. 82: 808–815.
- Zhao, S., White, D.G., Ge, B., Ayers, S., Friedman, S., English, L., Wagner, D., Gaines, S., Meng, J. (2001). Identification and characterization of integron-mediated antibiotic resistance among shiga toxin-producing Escherichia coli isolates. Appl. Environ. Microbiol. 67: 1558–1564.