ORIGINAL RESEARCH
Assessing the Biocontrol Potential of Some
Isolated Bacteriophages Against Salmonella spp.
in Food Preservation: A Preliminary Study
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1
Department of Chemistry, Faculty of Science, Cairo University, Cairo, Egypt
2
Animal Production Department, Food and Agriculture Sciences College, King Saud University, Riyadh, Saudi Arabia
3
Toxicology and Mycotoxin Research Unit, U.S. National Poultry Research Center, Agricultural Research Service, U.S.
Department of Agriculture, Athens, GA, United States
4
The Regional Center for Mycology and Biotechnology, Al-Azhar University, Nasr City, Cairo, Egypt
Submission date: 2024-01-18
Final revision date: 2024-03-10
Acceptance date: 2024-05-19
Online publication date: 2024-09-04
Publication date: 2025-04-04
Corresponding author
Mohammed Yosri
The Regional Center for Mycology and Biotechnology, Al-Azhar University, Nasr City, Cairo, Egypt
Pol. J. Environ. Stud. 2025;34(4):3763-3777
KEYWORDS
TOPICS
ABSTRACT
Food- and water-borne illnesses caused by Salmonella spp. are one of the pandemic loads
in developing nations and are seen as a sign of poor food and water cleanliness. In the early 20th
century, bacteriophages were often utilized to treat various bacterial illnesses, but their significance
declined after the development of pharmaceutical antibiotics. The resurgence of several microorganisms
with antibiotic resistance has sparked new interest in this field of study. This research was done
to evaluate the effectiveness of domestically acquired bacteriophages utilized as effective bio-control
agents and Salmonella spp. detection methods. Using the enhanced culture approach, 28 phages
were recovered from environmental materials. Host range analysis, restriction analysis, pulsed-field
gel electrophoresis (PFGE), and transmission electron microscopy were used to characterize some
of the isolated phages. Isolated phages may have the potential to be a safe and efficient substitute for
antibiotics in the fight against Salmonella infection in the food business since they can be used to
biocontrol the bacterium Salmonella for food preservation without changing the natural flora of the
gastrointestinal tract. The CUMR17 phage from the family Siphoviridae was chosen due to its size
for the biocontrol of Salmonella spp. in chicken meat and milk at 4ºC and 25ºC, with a constant
and powerful biocontrol impact even prior to 24 hours at 4ºC. The findings may be used to create
a biocontrol agent that avoids Salmonella infection in the food sector, making food safer in impoverished
nations.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (57)
8.
JONES J.B., VALLAD G.E., IRIARTE F.B., OBRADOVIĆ A., WERNSING M.H., JACKSON L.E., BALOGH B., HONG J.C., MOMOL M.T. Considerations for using bacteriophages for plant disease control. Bacteriophage. 2 (4), 208, 2012.
https://doi.org/10.4161/bact.2... https://doi.org/10.4161/bact.2... PMid:23531902 PMCid:PMC3594208.
10.
SHANG Y., SUN Q., CHEN H., WU Q., CHEN M., YANG S., DU M., ZHA F., YE Q., ZHANG J. Isolation and Characterization of a Novel Salmonella Phage vB_SalP_TR2. Frontiers in Microbiology. 12, 664810, 2021.
https://doi.org/10.3389/fmicb.... https://doi.org/10.3389/fmicb.... PMid:34234757 PMCid:PMC8256156.
12.
ZHAO J., LIN Y., WANG C., ZAYDA M., MAUNG A.T., MOHAMMADI T.N., DUC H.M., YU P., MA M., GONG D., SATO J., MASUDA Y., HONJOH K.I., MIYAMOTO T., ZENG Z. Biocontrol of Salmonella Typhimurium in milk, lettuce, raw pork meat and ready-to-eat steamed chicken breast by using a novel bacteriophage with broad host range. International Journal of Food Microbiology. 402, 110295, 2023.
https://doi.org/10.1016/j.ijfo... https://doi.org/10.1016/j.ijfo... PMid:37352774.
18.
CASTRO-MEJÍA J.L., MUHAMMED M.K., KOT W., NEVE H., FRANZ C.M., HANSEN L.H., VOGENSEN F.K., NIELSEN D.S. Optimizing protocols for extraction of bacteriophages prior to metagenomic analyses of phage communities in the human gut. Microbiome. 3, 64, 2015.
https://doi.org/10.1186/s40168... https://doi.org/10.1186/s40168... PMid:26577924 PMCid:PMC4650499.
21.
CROSS T., SCHOFF C., CHUDOFF D., GRAVES L., BROOMELL H., TERRY K., FARINA J., CORREA A., SHADE D., DUNBAR D. An optimized enrichment technique for the isolation of Arthrobacter bacteriophage species from soil sample isolates. Journal of Visualized Experiments. 98, 52781, 2015.
https://doi.org/10.3791/52781 https://doi.org/10.3791/52781.
24.
MHONE A.L., MAKUMI A., ODABA J., GUANTAI L., GUNATHILAKE K.M.D., LOIGNON S., NGUGI C.W., AKHWALE J.K., MOINEAU S., SVITEK N. Salmonella enteritidis Bacteriophages Isolated from Kenyan Poultry Farms Demonstrate Time-Dependent Stability in Environments Mimicking the Chicken Gastrointestinal Tract. Viruses. 14 (8), 1788, 2022.
https://doi.org/10.3390/v14081... https://doi.org/10.3390/v14081... PMid:36016410 PMCid:PMC9416366.
27.
GONZÁLEZ-VILLALOBOS E., RIBAS-APARICIO R.M., MONTEALEGRE G.E.R., BELMONT-MONROY L., ORTEGA-GARCÍA Y., APARICIO-OZORES G., BALCÁZAR J.L., ESLAVA-CAMPOS C.A., HERNÁNDEZ-CHIÑAS U., MOLINA-LÓPEZ J. Isolation and characterization of novel bacteriophages as a potential therapeutic option for Escherichia coli urinary tract infections. Applied Microbiology and Biotechnology. 105 (13), 5617, 2021.
https://doi.org/10.1007/s00253... https://doi.org/10.1007/s00253... PMid:34254156 PMCid:PMC8285336.
28.
SAMBROOK J., FRITSCH E.F., MANIATIS T. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, 1989.
29.
JAIMIPAK T., YOKSAN S., UBOL S., PULMANAUSAHAKUL R. Small plaque size variant of chikungunya primary isolate showed reduced virulence in mice. Asian Pacific Journal of Allergy and Immunology. 36 (3), 201, 2018.
https://doi.org/10.12932/AP-20....
30.
JAIMIPUK T., SACHDEV S., YOKSAN S., THEPPARIT C. A Small-Plaque Isolate of the Zika Virus with Envelope Domain III Mutations Affect Viral Entry and Replication in Mammalian but Not Mosquito Cells. Viruses. 14, 480, 2022.
https://doi.org/10.3390/v14030... PMid:35336887 PMCid:PMC8954177.
31.
HAQ I.U., CHAUDHRY W.N., AKHTAR M.N., ANDLEEB S., QADRI I. Bacteriophages and their implications on future biotechnology: a review. Journal of Virology. 10 (9), 9, 2012.
https://doi.org/10.1186/1743-4... PMid:22234269 PMCid:PMC3398332.
33.
ROGOVSKI P., CADAMURO R.D., DA SILVA R., DE SOUZA E.B., BONATTO C., VIANCELLI A., MICHELON W., ELMAHDY E.M., TREICHEL H., RODRÍGUEZ-LÁZARO D., FONGARO G. Uses of Bacteriophages as Bacterial Control Tools and Environmental Safety Indicators. Frontiers in Microbiology. 12, 2021.
https://doi.org/10.3389/fmicb.... PMid:34917066 PMCid:PMC8670004.
35.
SHAO Y., WANG I.N. Bacteriophage adsorption rate and optimal lysis time. Genetics. 180 (1), 471, 2008.
https://doi.org/10.1534/geneti... PMid:18757924 PMCid:PMC2535697.
36.
VANDAMME E.J., MORTELMANS K. A century of bacteriophage research and applications: impacts on biotechnology, health, ecology and the economy. Journal of Chemistry & Technology and Biotechnology. 94, 323, 2019.
https://doi.org/10.1002/jctb.5....
37.
LEFKOWITZ E.J., DEMPSEY D.M., HENDRICKSON R.C., ORTON R.J., SIDDELL S.G., SMITH D.B. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Research. 46 (D1), D708, 2018.
https://doi.org/10.1093/nar/gk... PMid:29040670 PMCid:PMC5753373.
38.
WALKER S.J., ARCHER P., BANKS J.G. Growth of Listeria monocytogenes at refrigeration temperatures. Journal of Applied Bacteriology. 68, 157, 1990.
https://doi.org/10.1111/j.1365... PMid:2108109.
39.
TOKMAN J.I., KENT D.J., WIEDMANN M., DENES T. Temperature Significantly Affects the Plaquing and Adsorption Efficiencies of Listeria Phages. Frontiers in Microbiology. 3 (7), 631, 2016.
https://doi.org/10.3389/fmicb.... PMid:27199957 PMCid:PMC4853374.
40.
WÓJCIK E.A., STAŃCZYK M., WOJTASIK A., KOWALSKA J.D., NOWAKOWSKA M., ŁUKASIAK M., BARTNICKA M., KAZIMIERCZAK J., DASTYCH J. Comprehensive evaluation of the safety and efficacy of BAFASAL® bacteriophage preparation for the reduction of Salmonella in the food chain. Viruses. 12 (7), 742, 2020.
https://doi.org/10.3390/v12070... PMid:32664206 PMCid:PMC7412135.
42.
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. Poultry Science. 84 (7), 1141, 2005.
https://doi.org/10.1093/ps/84.... PMid:16050131.
43.
HAGENS S., LOESSNER M.J. Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Current Pharmaceutical Biotechnology. 11, 58, 2010.
https://doi.org/10.2174/138920... PMid:20214608.
44.
GUENTHER S., HERZIG O., FIESELER L., KLUMPP J., LOESSNER M.J. Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. International Journal of Food Microbiology. 154, 66, 2012.
https://doi.org/10.1016/j.ijfo... PMid:22244192.
45.
HUNGARO H.M., MENDONÊA R.C.S., GOUVÇA D.M., VANETTI M.C.D., PINTO C.L.O. Use of bacteriophages to reduce Salmonella in chicken skin in comparison with chemical agents. Food Research International. 52 (75), 81, 2013.
https://doi.org/10.1016/j.food....
46.
GRANT A.Q., PARVEEN S., SCHWARZ J., HASHEM F., VIMINI B. Reduction of Salmonella in ground chicken using a bacteriophage. Poultry Science. 96, 2845, 2017.
https://doi.org/10.3382/ps/pex... PMid:28371846.
47.
GUNATHILAKA G.U., TAHLAN V., MAFIZ A.I., POLUR M., ZHANG Y. Phages in urban wastewater have the potential to disseminate antibiotic resistance. International Journal of Antimicrobial Agents. 50, 678, 2017.
https://doi.org/10.1016/j.ijan... PMid:28803933.
48.
HARADA L.K., SILVA E.C., CAMPOS W.F., DEL FIOL F.S., VILA M., DĄBROWSKA K., KRYLOV V.N., BALCÃO V.M. Biotechnological applications of bacteriophages: state of the art. Microbiology Research. 212 (213), 38, 2018.
https://doi.org/10.1016/j.micr... PMid:29853167.
49.
ISLAM M.S., ZHOU Y., LIANG L., NIME I., LIU K., YAN T., WANG X., LI J. Application of a phage cocktail for control of Salmonella in foods and reducing biofilms. Viruses. 11, 841, 2019.
https://doi.org/10.3390/v11090... PMid:31510005 PMCid:PMC6784009.
50.
ACKERMANN H.W. Siphoviridae: Tailed bacteriophages: the order caudovirales. Advances in Virus Research. 51, 135, 1998.
https://doi.org/10.1016/S0065-... PMid:9891587 PMCid:PMC7173057.
51.
MILLER E.S., KUTTER E., MOSIG G., ARISAKA F., KUNISAWA T., RÜGER W. Myoviridae Bacteriophage T4 Genome. Microbiology and Molecular Biology Reviews. 67 (1), 86, 2003.
https://doi.org/10.1128/MMBR.6... PMid:12626685 PMCid:PMC150520.
52.
CASJENS S.R., THUMAN-COMMIKE P.A. Evolution of Mosaically Related Tailed Bacteriophage Genomes Seen Through the Lens of Phage P22 Virion Assembly. Virology. 411 (2), 393, 2003.
https://doi.org/10.1016/j.viro... PMid:21310457.
53.
TOMAT D., MIGLIORE L., AQUILI V., QUIBERONI A., BALAGUE C. Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli in meat products. Frontiers of Cellular and Infection Microbiology. 3 (20), 1, 2013.
https://doi.org/10.3389/fcimb.... PMid:23761050 PMCid:PMC3674477.
54.
YEH Y., PURUSHOTHAMAN P., GUPTA N., RAGNONE M., VERMA S.C., DE MELLO A.S. Bacteriophage application on red meats and poultry: effects on Salmonella population in final ground products. Meat Science. 127 (30), 34, 2017.
https://doi.org/10.1016/j.meat... PMid:28110127.
55.
MERIKANTO I., LAAKSO J., KAITALA V. Outside-host phage therapy as a biological control against environmental infectious diseases. Theoretical Biology and Medical Modelling. 15 (1), 7, 2018.
https://doi.org/10.1186/s12976... PMid:29879998 PMCid:PMC5992827.
56.
DUC H.M., SON H.M., HONJOH K., MIYAMOTO T. Isolation and application of bacteriophages to reduce Salmonella contamination in raw chicken meat. LWT Food Science and Technology. 91, 353, 2018.
https://doi.org/10.1016/j.lwt.....
57.
GE H., FU S., GUO H., HU M., XU Z., ZHOU X., CHEN X., JIAO X. Application and challenge of bacteriophage in the food protection. International Journal of Food Microbiology. 380, 109872, 2022.
https://doi.org/10.1016/j.ijfo... PMid:35981493.