A Lytic Bacteriophage PS2 with Potential for Controlling Salmonella infections in Chickens and Ducks
Main Article Content
Abstract
Salmonella is one of the most common and dangerous pathogens, causing significant economic losses to the poultry industry worldwide. It is also a leading cause of foodborne diseases in both humans and animals. To control Salmonella infections, antibiotics are frequently used. In Vietnam, antibiotics are administered not only for disease prevention and treatment but also as growth promoters in livestock. This practice has contributed to the emergence and spread of antibiotic-resistant bacterial strains. Additionally, antibiotic residues in poultry products, such as eggs and meat, pose direct and indirect risks to human. Recently, phage therapy has been explored as a promising alternative to antibiotics for the prevention and treatment of bacterial infections, particularly those caused by antibiotic-resistant strains. In this study, we describe the isolation, selection, and biological characterization of a bacteriophage strain with strong lytic activity against Salmonella enterica subsp. enterica, a causative agent of diarrhea in chickens and ducks in Hai Duong province, Vietnam. The isolated phage strain, PS2, exhibited specific lytic activity against Salmonella and was capable of lysing all 30 tested Salmonella strains. Morphologically, PS2 has Myovirus-like morphology with an icosahedral head of 80.02 ± 3 nm in diameter and a long straight tail of 90.6 ± 8 nm in length. PS2 demonstrated an optimal multiplicity of infection (MOI) of 0.01, a latent phase of approximately 25 minutes, and a burst size of about 225 plaque-forming units (PFU) per cell. Moreover, PS2 maintained stable biological activity across a temperature range of -20 °C to 60 °C and remained stable within a pH range of 5 to 12. Taken together, these results suggest that PS2 is a promising candidate for the development of phage therapy to combat Salmonella infections in poultry in Vietnam.
Keywords:
Bacteriophages, diarrhea syndrome, poultry industry, Salmonella, Salmonellosis.
References
[1] C. Bâtie, E. Loire, D. B. Truong, H. M. Tuan, N. T. K. Cuc, M. Paul, F. Goutard, Characterisation of Chicken Farms in Vietnam: A Typology of Antimicrobial Use Among Different Production Systems. Preventive Veterinary Medicine, Vol. 208, 2022, pp. 105731.
[2] Thames, A. T. Sukumaran, A Review of Salmonella and Campylobacter in Broiler Meat: Emerging Challenges and Food Safety Measures, Foods, Vol. 9, No. 6, 2020, pp. 776.
[3] K. Wessels, D. Rip, P. Gouws, Salmonella in Chicken Meat: Consumption, Outbreaks, Characteristics, Current Control Methods and the Potential of Bacteriophage Use. Foods (Basel, Switzerland), Vol. 10, No. 8, 2021, pp. 1742-1762.
[4] L. Chappell, P. Kaiser, P. Barrow, M. A. Jones, C. Johnston, P. Wigley, The Immunobiology of Avian Systemic Salmonellosis. Veterinary Immunology and Immunopathology, Vol. 128, 2009, pp. 53-59.
[5] M. T. E. Saadony, H. M. Salem, A. M. E. Tahan, T. A. A. E. Mageed, S. M. Soliman, A. F. Khafaga, A. A. Swelum, A. E. Ahmed, F. A. Alshammari, M. E. A. E. Hack, The Control of Poultry Salmonellosis Using Organic Agents: An Updated Overview. Poultry Science, Vol. 101, No. 4, 2022, pp. 101716.
[6] S. L. Foley, T. J. Johnson, S. C. Ricke, R. Nayak, J. Danzeisen, Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars. Microbiology and Molecular Biology Reviews, Vol. 77, No. 4, 2013, pp. 582-607.
[7] P. Barrow, O. F. Neto, Pullorum Disease And Fowl Typhoid-New Thoughts on Old Diseases: A Review. Avian Pathology, Vol. 40, No. 1, 2011, pp. 1-13.
[8] J. J. C. Mas, M. Choisy, N. Van Cuong, G. Thwaites, S. Baker, An Estimation of Total Antimicrobial Usage in Humans and Animals in Vietnam, Antimicrobial Resistance & Infection Control, Vol. 9, 2020, pp. 1-6.
[9] M. S. Mahmud, M. L. Bari, M. A. Hossain, Prevalence of Salmonella Serovars and Antimicrobial Resistance Profiles in Poultry of Savar Area, Bangladesh, Foodborne Pathogens and Disease, Vol. 8, No. 10, 2011, pp. 1111-1118.
[10] L. Andoh, A. Dalsgaard, K. O. Danso, M. Newman, L. Barco, J. Olsen, Prevalence and Antimicrobial Resistance of Salmonella Serovars Isolated from Poultry in Ghana, Epidemiology & Infection, Vol. 144, No. 15, 2016, pp. 3288-3299.
[11] V. M. Duc, Y. Nakamoto, A. Fujiwara, H. Toyofuku, T. Obi, T. Chuma, Prevalence of Salmonella in Broiler Chickens in Kagoshima, Japan in 2009 to 2012 and the Relationship Between Serovars Changing and Antimicrobial Resistance, BMC Veterinary Research, Vol. 15, 2019, pp. 1-8.
[12] A. Nelson, S. Manandhar, J. Ruzante, A. Gywali, B. Dhakal, S. Dulal, R. Chaulaga, S. M. Dixit, Antimicrobial Drug Resistant Non-Typhoidal Salmonella Enterica in Commercial Poultry Value Chain in Chitwan, Nepal, One Health Outlook, Vol. 2, 2020, pp. 1-8.
[13] N. S. Karabasanavar, C. B. Madhavaprasad, S. A. Gopalakrishna, J. Hiremath, G. S. Patil, S. B Barbuddhe, Prevalence of Salmonella Serotypes S. Enteritidis and S. Typhimurium in Poultry and Poultry Products, Journal of Food Safety, Vol. 40, No. 6, 2020, pp. e12852.
[14] X. Wang, H. Wang, T. Li, F. Liu, Y. Cheng, X. Guo, G. Wen, Q. Luo, H. Shao, Z. Pan, Characterization of Salmonella spp. Isolated from Chickens in Central China, BMC Veterinary Research, Vol. 16, 2020, pp. 1-9.
[15] D. X. Binh, D. T. M. Lan, P. T. P. Lan, N. N. Minh, Prevalence and Virulence Gene of Salmonella Strains Isolated from Ducks in North Vietnam. Suranaree Journal of Science & Technology, Vol. 27, No. 1, 2020, pp. 1-9.
[16] T. K. Nguyen, L. T. Nguyen, T. T. Chau, T. T. Nguyen, B. N. Tran, T. Taniguchi, H. Hayashidani, K. T. Ly, Prevalence and Antibiotic Resistance of Salmonella Isolated from Poultry and Its Environment in the Mekong Delta, Vietnam. Veterinary World, Vol. 14, No. 12, 2021, pp. 3216.
[17] Y. H. Xuan, T. N. Khanh, K. L. T. Lien, Study on Salmonella spp. in Chicken and Environment from Households in Vinh Long Province, Can Tho University Journal of Science, Vol. 55, No. 6, 2019, pp. 1-6.
[18] A. A. E. Wahab, S. Basiouni, H. R. E. Seedi, M. F. Ahmed, L. R. Bielke, B. Hargis, G. T. Isaias, W. Eisenreich, H. Lehnherr, S. Kittler, An Overview of the Use of Bacteriophages in the Poultry Industry: Successes, Challenges, and Possibilities for Overcoming Breakdowns, Frontiers in Microbiology, Vol. 14, 2023, pp. 1136638.
[19] B. Rahman, M. Wasfy, M. Maksoud, N. Hanna, E. Dueger, B. House, Multi-drug Resistance and Reduced Susceptibility to Ciprofloxacin among Salmonella Enterica Serovar Typhi Isolates from the Middle East and Central Asia, New Microbes and New Infections, Vol. 2, No. 4, 2014, pp. 88-92.
[20] S. Fister, P. Mester, A. K. Witte, J. Sommer, D. Schoder, P. Rossmanith, Part of the Problem or The Solution? Indiscriminate Use of Bacteriophages in the Food Industry Can Reduce Their Potential and Impair Growth-Based Detection Methods, Trends in Food Science & Technology, Vol. 90, 2019, pp. 170-174.
[21] C. Pereira, C. Moreirinha, M. Lewicka, P. Almeida, C. Clemente, Â. Cunha, I. Delgadillo, J. L. Romalde, M. L. Nunes, A. Almeida, Bacteriophages with Potential to Inactivate Salmonella Typhimurium: Use of Single Phage Suspensions and Phage Cocktails. Virus Research, Vol. 220, 2016, pp. 179-192.
[22] B. M. Rao, K. Lalitha, Bacteriophages for Aquaculture: Are They Beneficial or Inimical, Aquaculture, Vol. 437, 2015, pp. 146-154.
[23] E. F. S. Authority, The European Union One Health 2018 Zoonoses Report, EFSA Journal, Vol. 17, No. 12, 2019, pp. e05926.
[24] K. Żbikowska, M. Michalczuk, B. Dolka, The Use of Bacteriophages in the Poultry Industry, Animals, Vol. 10, No. 5, 2020, pp. 872.
[25] R. Ranjbar, S. M. Mortazavi, A. M. Tavana, M. Sarshar, A. Najafi, R. S. Zanjani, Simultaneous Molecular Detection of Salmonella Enterica Serovars Typhi, Enteritidis, Infantis, and Typhimurium, Iranian Journal of Public Health, Vol. 46, No. 1, 2017, pp. 103-111.
[26] S. T. Abedon, Bacteriophage Clinical Use as Antibacterial “Drugs”: Utility and Precedent, Bugs as Drugs: Therapeutic Microbes for the Prevention and Treatment of Disease, 2018, pp. 417-451.
[27] C. Lukman, C. Yonathan, S. Magdalena, D. E. Waturangi, Isolation and Characterization of Pathogenic Escherichia coli Bacteriophages from Chicken and Beef Offal, BMC Research Notes, Vol. 13, 2020, pp. 1-7.
[28] Y. Shimamori, A. K. Pramono, T. Kitao, T. Suzuki, S. I. Aizawa, T. Kubori, H. Nagai, S. Takeda,
H. Ando, Isolation and Characterization of a Novel Phage SaGU1 That Infects Staphylococcus Aureus Clinical Isolates from Patients with Atopic Dermatitis, Current Microbiology, Vol. 78, 2021, pp. 1267-1276.
[29] S. Sinha, R. K. Grewal, S. Roy, Modeling Bacteria-Phage Interactions and Its Implications for Phage Therapy, In Advances in Applied Microbiology, Vol. 103, 2018, pp. 103-141.
[30] M. A. S. Khan, S. R. Rahman, Use of Phages to Treat Antimicrobial-Resistant Salmonella Infections in Poultry, Veterinary Sciences, Vol. 9, No. 8, 2022, pp. 438.
[31] C. L. Carrillo, S. T. Abedon, Pros and Cons of Phage Therapy, Bacteriophage, Vol. 1, No. 2, 2011, pp. 111-114.
[32] R. B. Montenegro, R. García, F. Dueñas, D. Rivera, A. O. Capurro, S. Erickson, A. I. M. Switt, Comparative Analysis of Felixounavirus Genomes Including Two New Members of the Genus that Infect Salmonella Infantis, Antibiotics (Basel), Vol. 10, No. 7, 2021, pp. 806.
[33] S. Bhandare, O. U. Lawal, A. Colavecchio, B. Cadieux, Y. Z. Jovich, Z. Zhong, E. Tompkins, M. Amitrano, I. K. Ibrulj, B. Boyle, S. Wang, R. C. Levesque, P. Delaquis, M. Danyluk, L. Goodridge, Genomic and Phenotypic Analysis of Salmonella Enterica Bacteriophages Identifies Two Novel Phage Species. Microorganisms, Vol. 12, No. 4, 2024, pp. 695.
[34] A. Unverdi, H. B. Erol, B. Kaskatepe, O. Babacan, Characterization of Salmonella Phages Isolated from Poultry Coops and Its Effect with Nisin on Food Bio‐Control, Food Science & Nutrition, Vol. 12, No. 4, 2024, pp. 2760-2771.
[35] L. M. Kasman, L. D. Porter, Bacteriophages, In StatPearls, StatPearls Publishing, 2022.
[36] Y. Zhang, Y. Ding, W. Li, W. Zhu, J. Wang, X. Wang, Application of a Novel Lytic Podoviridae Phage Pu20 for Biological Control of Drug-Resistant Salmonella in Liquid Eggs, Pathogens, Vol. 10, No. 1, 2021, pp. 34.
[37] Y. Wang, J. Wu, J. Li, C. Yu, J. Gao, F. Song, L. Zhou, R. Zhang, S. Jiang, Y. Zhu, Isolation and Characterization of Duck Sewage Source Salmonella Phage P6 and Antibacterial Activity for Recombinant Endolysin LysP6, Poultry Science, Vol. 103, No. 11, 2024, pp. 104227.
[38] M. A. S. Khan, Z. Islam, C. Barua, M. M. H. Sarkar, M. F. Ahmed, S. R. Rahman, Phenotypic Characterization and Genomic Analysis of a Salmonella Phage L223 for Biocontrol of Salmonella spp. in Poultry. Scientific Reports,
Vol. 14, No. 1, 2024, pp. 15347.
[39] S. Abedon, E. Bartom, Multiplicity of Infection, In Brenner's Encyclopedia of Genetics: Second Edition, Elsevier Inc, 2013, pp. 509-510.
[40] S. Cao, W. Yang, X. Zhu, C. Liu, J. Lu, Z. Si, L. Pei, L. Zhang, W. Hu, Y. Li, Isolation and Identification of the Broad-Spectrum High-Efficiency Phage vB_SalP_LDW16 and Its Therapeutic Application in Chickens, BMC Veterinary Research, Vol. 18, No. 1, 2022, pp. 386.
[41] Y. Li, P. Lv, D. Shi, H. Zhao, X. Yuan, X. Jin, X. Wang, A Cocktail of Three Virulent Phages Controls Multidrug-Resistant Salmonella Enteritidis Infection in Poultry, Frontiers in Microbiology, Vol. 13, 2022, pp. 940525.
[42] Y. Zhang, M. Chu, Y. T. Liao, A. Salvador, V. C. Wu, Characterization of Two Novel Salmonella Phages Having Biocontrol Potential Against Salmonella spp. in Gastrointestinal Conditions, Scientific Reports, Vol. 14, No. 1, 2024, pp. 12294.
[43] E. Jończyk, M. Kłak, R. Międzybrodzki, A. Górski, the Influence of External Factors on Bacteriophages, Folia Microbiologica, Vol. 56, 2011, pp. 191-200.
[44] M. Ye, M. Sun, D. Huang, Z. Zhang, H. Zhang, S. Zhang, F. Hu, X. Jiang, W. Jiao, A Review of Bacteriophage Therapy for Pathogenic Bacteria Inactivation in the Soil Environment, Environment international, Vol. 129, 2019, pp. 488-496.
[45] Z. Zhang, F. Yu, Y. Zou, Y. Qiu, A. Wu, T. Jiang, Y. Peng, Phage Protein Receptors Have Multiple Interaction Partners and High Expressions. Bioinformatics, Vol. 36, No. 10, 2020, pp. 2975-2979.
[46] Y. Ma, E. Li, Z. Qi, H. Li, X. Wei, W. Lin, R. Zhao, A. Jiang, H. Yang, Z. Yin, Isolation and Molecular Characterisation of Achromobacter Phage phiAxp-3, an N4-like Bacteriophage, Scientific Reports, Vol. 6, No. 1, 2016, pp. 24776.
[47] D. J. Malik, I. J. Sokolov, G. K. Vinner, F. Mancuso, S. Cinquerrui, G. T. Vladisavljevic,
M. R. Clokie, N. J. Garton, A. G. Stapley, A. Kirpichnikova, Formulation, Stabilisation and Encapsulation of Bacteriophage For Phage Therapy, Advances in Colloid and Interface Science, Vol. 249, 2017, pp. 100-133.
[48] H. Ge, Y. Xu, M. Hu, K. Zhang, S. Zhang, X. Chen, Isolation, Characterization, and Application in Poultry Products of a Salmonella-Specific Bacteriophage, S55, Journal of Food Protection, Vol. 84, No. 7, 2021, pp. 1202-1212.
[49] A. Pradeep, S. Ramasamy, J. Veniemilda, C. Kumar, Effect of pH & Temperature Variations on Phage Stability-a Crucial Prerequisite for Successful Phage Therapy, International Journal of Pharmaceutical Sciences and Research, Vol. 13, 2022, pp. 5178-5182.
[50] P. García, C. Madera, B. Martinez, A. Rodríguez, J. E. Suárez, Prevalence of Bacteriophages Infecting Staphylococcus Aureus in Dairy Samples and Their Potential as Biocontrol Agents, Journal of Dairy Science, Vol. 92, No. 7, 2009, pp. 3019-3026.
[51] H. Bao, H. Zhang, R. Wang, Isolation and Characterization of Bacteriophages of Salmonella Enterica Serovar Pullorum, Poultry Science, Vol. 90, No. 10, 2011, pp. 2370-2377.
[52] S. S. Hong, J. Jeong, J. Lee, S. Kim, W. Min, H. Myung, Therapeutic Effects of Bacteriophages Against Salmonella Gallinarum Infection in Chickens, Journal of Microbiology and Biotechnology, Vol. 23, No. 10, 2013, pp. 1478-1483.
[53] S. Sattar, M. Bailie, A. Yaqoob, S. Khanum, K. Fatima, A. U. R. B. Altaf, I. Ahmed, S. T. A. Shah, J. Munawar, Q. A. Zehra, Characterization of Two Novel Lytic Bacteriophages Having Lysis Potential Against MDR Avian Pathogenic Escherichia Coli Strains of Zoonotic Potential, Scientific reports, Vol. 13, No. 1, 2023, pp. 10043.
[2] Thames, A. T. Sukumaran, A Review of Salmonella and Campylobacter in Broiler Meat: Emerging Challenges and Food Safety Measures, Foods, Vol. 9, No. 6, 2020, pp. 776.
[3] K. Wessels, D. Rip, P. Gouws, Salmonella in Chicken Meat: Consumption, Outbreaks, Characteristics, Current Control Methods and the Potential of Bacteriophage Use. Foods (Basel, Switzerland), Vol. 10, No. 8, 2021, pp. 1742-1762.
[4] L. Chappell, P. Kaiser, P. Barrow, M. A. Jones, C. Johnston, P. Wigley, The Immunobiology of Avian Systemic Salmonellosis. Veterinary Immunology and Immunopathology, Vol. 128, 2009, pp. 53-59.
[5] M. T. E. Saadony, H. M. Salem, A. M. E. Tahan, T. A. A. E. Mageed, S. M. Soliman, A. F. Khafaga, A. A. Swelum, A. E. Ahmed, F. A. Alshammari, M. E. A. E. Hack, The Control of Poultry Salmonellosis Using Organic Agents: An Updated Overview. Poultry Science, Vol. 101, No. 4, 2022, pp. 101716.
[6] S. L. Foley, T. J. Johnson, S. C. Ricke, R. Nayak, J. Danzeisen, Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars. Microbiology and Molecular Biology Reviews, Vol. 77, No. 4, 2013, pp. 582-607.
[7] P. Barrow, O. F. Neto, Pullorum Disease And Fowl Typhoid-New Thoughts on Old Diseases: A Review. Avian Pathology, Vol. 40, No. 1, 2011, pp. 1-13.
[8] J. J. C. Mas, M. Choisy, N. Van Cuong, G. Thwaites, S. Baker, An Estimation of Total Antimicrobial Usage in Humans and Animals in Vietnam, Antimicrobial Resistance & Infection Control, Vol. 9, 2020, pp. 1-6.
[9] M. S. Mahmud, M. L. Bari, M. A. Hossain, Prevalence of Salmonella Serovars and Antimicrobial Resistance Profiles in Poultry of Savar Area, Bangladesh, Foodborne Pathogens and Disease, Vol. 8, No. 10, 2011, pp. 1111-1118.
[10] L. Andoh, A. Dalsgaard, K. O. Danso, M. Newman, L. Barco, J. Olsen, Prevalence and Antimicrobial Resistance of Salmonella Serovars Isolated from Poultry in Ghana, Epidemiology & Infection, Vol. 144, No. 15, 2016, pp. 3288-3299.
[11] V. M. Duc, Y. Nakamoto, A. Fujiwara, H. Toyofuku, T. Obi, T. Chuma, Prevalence of Salmonella in Broiler Chickens in Kagoshima, Japan in 2009 to 2012 and the Relationship Between Serovars Changing and Antimicrobial Resistance, BMC Veterinary Research, Vol. 15, 2019, pp. 1-8.
[12] A. Nelson, S. Manandhar, J. Ruzante, A. Gywali, B. Dhakal, S. Dulal, R. Chaulaga, S. M. Dixit, Antimicrobial Drug Resistant Non-Typhoidal Salmonella Enterica in Commercial Poultry Value Chain in Chitwan, Nepal, One Health Outlook, Vol. 2, 2020, pp. 1-8.
[13] N. S. Karabasanavar, C. B. Madhavaprasad, S. A. Gopalakrishna, J. Hiremath, G. S. Patil, S. B Barbuddhe, Prevalence of Salmonella Serotypes S. Enteritidis and S. Typhimurium in Poultry and Poultry Products, Journal of Food Safety, Vol. 40, No. 6, 2020, pp. e12852.
[14] X. Wang, H. Wang, T. Li, F. Liu, Y. Cheng, X. Guo, G. Wen, Q. Luo, H. Shao, Z. Pan, Characterization of Salmonella spp. Isolated from Chickens in Central China, BMC Veterinary Research, Vol. 16, 2020, pp. 1-9.
[15] D. X. Binh, D. T. M. Lan, P. T. P. Lan, N. N. Minh, Prevalence and Virulence Gene of Salmonella Strains Isolated from Ducks in North Vietnam. Suranaree Journal of Science & Technology, Vol. 27, No. 1, 2020, pp. 1-9.
[16] T. K. Nguyen, L. T. Nguyen, T. T. Chau, T. T. Nguyen, B. N. Tran, T. Taniguchi, H. Hayashidani, K. T. Ly, Prevalence and Antibiotic Resistance of Salmonella Isolated from Poultry and Its Environment in the Mekong Delta, Vietnam. Veterinary World, Vol. 14, No. 12, 2021, pp. 3216.
[17] Y. H. Xuan, T. N. Khanh, K. L. T. Lien, Study on Salmonella spp. in Chicken and Environment from Households in Vinh Long Province, Can Tho University Journal of Science, Vol. 55, No. 6, 2019, pp. 1-6.
[18] A. A. E. Wahab, S. Basiouni, H. R. E. Seedi, M. F. Ahmed, L. R. Bielke, B. Hargis, G. T. Isaias, W. Eisenreich, H. Lehnherr, S. Kittler, An Overview of the Use of Bacteriophages in the Poultry Industry: Successes, Challenges, and Possibilities for Overcoming Breakdowns, Frontiers in Microbiology, Vol. 14, 2023, pp. 1136638.
[19] B. Rahman, M. Wasfy, M. Maksoud, N. Hanna, E. Dueger, B. House, Multi-drug Resistance and Reduced Susceptibility to Ciprofloxacin among Salmonella Enterica Serovar Typhi Isolates from the Middle East and Central Asia, New Microbes and New Infections, Vol. 2, No. 4, 2014, pp. 88-92.
[20] S. Fister, P. Mester, A. K. Witte, J. Sommer, D. Schoder, P. Rossmanith, Part of the Problem or The Solution? Indiscriminate Use of Bacteriophages in the Food Industry Can Reduce Their Potential and Impair Growth-Based Detection Methods, Trends in Food Science & Technology, Vol. 90, 2019, pp. 170-174.
[21] C. Pereira, C. Moreirinha, M. Lewicka, P. Almeida, C. Clemente, Â. Cunha, I. Delgadillo, J. L. Romalde, M. L. Nunes, A. Almeida, Bacteriophages with Potential to Inactivate Salmonella Typhimurium: Use of Single Phage Suspensions and Phage Cocktails. Virus Research, Vol. 220, 2016, pp. 179-192.
[22] B. M. Rao, K. Lalitha, Bacteriophages for Aquaculture: Are They Beneficial or Inimical, Aquaculture, Vol. 437, 2015, pp. 146-154.
[23] E. F. S. Authority, The European Union One Health 2018 Zoonoses Report, EFSA Journal, Vol. 17, No. 12, 2019, pp. e05926.
[24] K. Żbikowska, M. Michalczuk, B. Dolka, The Use of Bacteriophages in the Poultry Industry, Animals, Vol. 10, No. 5, 2020, pp. 872.
[25] R. Ranjbar, S. M. Mortazavi, A. M. Tavana, M. Sarshar, A. Najafi, R. S. Zanjani, Simultaneous Molecular Detection of Salmonella Enterica Serovars Typhi, Enteritidis, Infantis, and Typhimurium, Iranian Journal of Public Health, Vol. 46, No. 1, 2017, pp. 103-111.
[26] S. T. Abedon, Bacteriophage Clinical Use as Antibacterial “Drugs”: Utility and Precedent, Bugs as Drugs: Therapeutic Microbes for the Prevention and Treatment of Disease, 2018, pp. 417-451.
[27] C. Lukman, C. Yonathan, S. Magdalena, D. E. Waturangi, Isolation and Characterization of Pathogenic Escherichia coli Bacteriophages from Chicken and Beef Offal, BMC Research Notes, Vol. 13, 2020, pp. 1-7.
[28] Y. Shimamori, A. K. Pramono, T. Kitao, T. Suzuki, S. I. Aizawa, T. Kubori, H. Nagai, S. Takeda,
H. Ando, Isolation and Characterization of a Novel Phage SaGU1 That Infects Staphylococcus Aureus Clinical Isolates from Patients with Atopic Dermatitis, Current Microbiology, Vol. 78, 2021, pp. 1267-1276.
[29] S. Sinha, R. K. Grewal, S. Roy, Modeling Bacteria-Phage Interactions and Its Implications for Phage Therapy, In Advances in Applied Microbiology, Vol. 103, 2018, pp. 103-141.
[30] M. A. S. Khan, S. R. Rahman, Use of Phages to Treat Antimicrobial-Resistant Salmonella Infections in Poultry, Veterinary Sciences, Vol. 9, No. 8, 2022, pp. 438.
[31] C. L. Carrillo, S. T. Abedon, Pros and Cons of Phage Therapy, Bacteriophage, Vol. 1, No. 2, 2011, pp. 111-114.
[32] R. B. Montenegro, R. García, F. Dueñas, D. Rivera, A. O. Capurro, S. Erickson, A. I. M. Switt, Comparative Analysis of Felixounavirus Genomes Including Two New Members of the Genus that Infect Salmonella Infantis, Antibiotics (Basel), Vol. 10, No. 7, 2021, pp. 806.
[33] S. Bhandare, O. U. Lawal, A. Colavecchio, B. Cadieux, Y. Z. Jovich, Z. Zhong, E. Tompkins, M. Amitrano, I. K. Ibrulj, B. Boyle, S. Wang, R. C. Levesque, P. Delaquis, M. Danyluk, L. Goodridge, Genomic and Phenotypic Analysis of Salmonella Enterica Bacteriophages Identifies Two Novel Phage Species. Microorganisms, Vol. 12, No. 4, 2024, pp. 695.
[34] A. Unverdi, H. B. Erol, B. Kaskatepe, O. Babacan, Characterization of Salmonella Phages Isolated from Poultry Coops and Its Effect with Nisin on Food Bio‐Control, Food Science & Nutrition, Vol. 12, No. 4, 2024, pp. 2760-2771.
[35] L. M. Kasman, L. D. Porter, Bacteriophages, In StatPearls, StatPearls Publishing, 2022.
[36] Y. Zhang, Y. Ding, W. Li, W. Zhu, J. Wang, X. Wang, Application of a Novel Lytic Podoviridae Phage Pu20 for Biological Control of Drug-Resistant Salmonella in Liquid Eggs, Pathogens, Vol. 10, No. 1, 2021, pp. 34.
[37] Y. Wang, J. Wu, J. Li, C. Yu, J. Gao, F. Song, L. Zhou, R. Zhang, S. Jiang, Y. Zhu, Isolation and Characterization of Duck Sewage Source Salmonella Phage P6 and Antibacterial Activity for Recombinant Endolysin LysP6, Poultry Science, Vol. 103, No. 11, 2024, pp. 104227.
[38] M. A. S. Khan, Z. Islam, C. Barua, M. M. H. Sarkar, M. F. Ahmed, S. R. Rahman, Phenotypic Characterization and Genomic Analysis of a Salmonella Phage L223 for Biocontrol of Salmonella spp. in Poultry. Scientific Reports,
Vol. 14, No. 1, 2024, pp. 15347.
[39] S. Abedon, E. Bartom, Multiplicity of Infection, In Brenner's Encyclopedia of Genetics: Second Edition, Elsevier Inc, 2013, pp. 509-510.
[40] S. Cao, W. Yang, X. Zhu, C. Liu, J. Lu, Z. Si, L. Pei, L. Zhang, W. Hu, Y. Li, Isolation and Identification of the Broad-Spectrum High-Efficiency Phage vB_SalP_LDW16 and Its Therapeutic Application in Chickens, BMC Veterinary Research, Vol. 18, No. 1, 2022, pp. 386.
[41] Y. Li, P. Lv, D. Shi, H. Zhao, X. Yuan, X. Jin, X. Wang, A Cocktail of Three Virulent Phages Controls Multidrug-Resistant Salmonella Enteritidis Infection in Poultry, Frontiers in Microbiology, Vol. 13, 2022, pp. 940525.
[42] Y. Zhang, M. Chu, Y. T. Liao, A. Salvador, V. C. Wu, Characterization of Two Novel Salmonella Phages Having Biocontrol Potential Against Salmonella spp. in Gastrointestinal Conditions, Scientific Reports, Vol. 14, No. 1, 2024, pp. 12294.
[43] E. Jończyk, M. Kłak, R. Międzybrodzki, A. Górski, the Influence of External Factors on Bacteriophages, Folia Microbiologica, Vol. 56, 2011, pp. 191-200.
[44] M. Ye, M. Sun, D. Huang, Z. Zhang, H. Zhang, S. Zhang, F. Hu, X. Jiang, W. Jiao, A Review of Bacteriophage Therapy for Pathogenic Bacteria Inactivation in the Soil Environment, Environment international, Vol. 129, 2019, pp. 488-496.
[45] Z. Zhang, F. Yu, Y. Zou, Y. Qiu, A. Wu, T. Jiang, Y. Peng, Phage Protein Receptors Have Multiple Interaction Partners and High Expressions. Bioinformatics, Vol. 36, No. 10, 2020, pp. 2975-2979.
[46] Y. Ma, E. Li, Z. Qi, H. Li, X. Wei, W. Lin, R. Zhao, A. Jiang, H. Yang, Z. Yin, Isolation and Molecular Characterisation of Achromobacter Phage phiAxp-3, an N4-like Bacteriophage, Scientific Reports, Vol. 6, No. 1, 2016, pp. 24776.
[47] D. J. Malik, I. J. Sokolov, G. K. Vinner, F. Mancuso, S. Cinquerrui, G. T. Vladisavljevic,
M. R. Clokie, N. J. Garton, A. G. Stapley, A. Kirpichnikova, Formulation, Stabilisation and Encapsulation of Bacteriophage For Phage Therapy, Advances in Colloid and Interface Science, Vol. 249, 2017, pp. 100-133.
[48] H. Ge, Y. Xu, M. Hu, K. Zhang, S. Zhang, X. Chen, Isolation, Characterization, and Application in Poultry Products of a Salmonella-Specific Bacteriophage, S55, Journal of Food Protection, Vol. 84, No. 7, 2021, pp. 1202-1212.
[49] A. Pradeep, S. Ramasamy, J. Veniemilda, C. Kumar, Effect of pH & Temperature Variations on Phage Stability-a Crucial Prerequisite for Successful Phage Therapy, International Journal of Pharmaceutical Sciences and Research, Vol. 13, 2022, pp. 5178-5182.
[50] P. García, C. Madera, B. Martinez, A. Rodríguez, J. E. Suárez, Prevalence of Bacteriophages Infecting Staphylococcus Aureus in Dairy Samples and Their Potential as Biocontrol Agents, Journal of Dairy Science, Vol. 92, No. 7, 2009, pp. 3019-3026.
[51] H. Bao, H. Zhang, R. Wang, Isolation and Characterization of Bacteriophages of Salmonella Enterica Serovar Pullorum, Poultry Science, Vol. 90, No. 10, 2011, pp. 2370-2377.
[52] S. S. Hong, J. Jeong, J. Lee, S. Kim, W. Min, H. Myung, Therapeutic Effects of Bacteriophages Against Salmonella Gallinarum Infection in Chickens, Journal of Microbiology and Biotechnology, Vol. 23, No. 10, 2013, pp. 1478-1483.
[53] S. Sattar, M. Bailie, A. Yaqoob, S. Khanum, K. Fatima, A. U. R. B. Altaf, I. Ahmed, S. T. A. Shah, J. Munawar, Q. A. Zehra, Characterization of Two Novel Lytic Bacteriophages Having Lysis Potential Against MDR Avian Pathogenic Escherichia Coli Strains of Zoonotic Potential, Scientific reports, Vol. 13, No. 1, 2023, pp. 10043.