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Recent Trends in Salmonella Outbreaks and Emerging Technology for Biocontrol of Salmonella Using Phages in Foods: A Review

  • Oh, Jun-Hyun (Department of Plant and Food Sciences, Sangmyung University) ;
  • Park, Mi-Kyung (School of Food Science and Biotechnology, Kyungpook National University)
  • Received : 2017.10.30
  • Accepted : 2017.11.15
  • Published : 2017.12.28

Abstract

Salmonella is one of the principal causes of foodborne outbreaks. As traditional control methods have shown less efficacy against emerging Salmonella serotypes or antimicrobial-resistant Salmonella, new approaches have been attempted. The use of lytic phages for the biocontrol of Salmonella in the food industry has become an attractive method owing to the many advantages offered by the use of phages as biocontrol agents. Phages are natural alternatives to traditional antimicrobial agents; they have proven effective in the control of bacterial pathogens in the food industry, which has led to the development of different phage products. The treatment with specific phages in the food industry can prevent the decay of products and the spread of bacterial diseases, and ultimately promotes safe environments for animal and plant food production, processing, and handling. After an extensive investigation of the current literature, this review focuses predominantly on the efficacy of phages for the successful control of Salmonella spp. in foods. This review also addresses the current knowledge on the pathogenic characteristics of Salmonella, the prevalence of emerging Salmonella outbreaks, the isolation and characterization of Salmonella-specific phages, the effectiveness of Salmonella-specific phages as biocontrol agents, and the prospective use of Salmonella-specific phages in the food industry.

Keywords

References

  1. Eng SK, Pusparajah P, Ab Nurul-Syakima M, Ser HL, Chan KG, Lee LH. 2015. Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front. Life Sci. 8: 284-293. https://doi.org/10.1080/21553769.2015.1051243
  2. Behravesh CB, Jones TF, Vugia DJ, Long C, Marcus R, Smith K, et al. 2011. Deaths associated with bacterial pathogens transmitted commonly through food: Foodborne Diseases Active Surveillance Network (FoodNet), 1996-2005. J. Infect. Dis. 204: 263-267. https://doi.org/10.1093/infdis/jir263
  3. Centers for Disease Control and Prevention (CDC). 2014. Number of deaths and case fatality ratio by pathogen. Available from http://www.cdc.go/foodnet/trends/2014/number-of-deathscfr-by-pathogen-2014.htmL.
  4. Olaimat AN, Holley RA. 2012. Factors influencing the microbial safety of fresh produce: a review. Food Microbiol. 32: 1-19. https://doi.org/10.1016/j.fm.2012.04.016
  5. Park MK, Park JW, Wikle HC, Chin BA. 2013. Evaluation of phage-based magnetoelastic biosensors for direct detection of Salmonella Typhimurium on spinach leaves. Sens. Actuators B Chem. 176: 1134-1140. https://doi.org/10.1016/j.snb.2012.10.084
  6. Handley JA, Hanning I, Ricke SC, Johnson MG, Jones FT, Apple RO. 2010. Temperature and bacterial profile of post chill poultry carcasses stored in processing combo held at room temperature. J. Food Sci. 75: M515-M520. https://doi.org/10.1111/j.1750-3841.2010.01790.x
  7. Valadez A, Lana C, Tu S-I, Morgan M, Bhunia A. 2009. Evanescent wave fiber optic biosensor for Salmonella detection in food. Sensors 9: 5810. https://doi.org/10.3390/s90705810
  8. Bao H, Zhang P, Zhang H, Zhou Y, Zhang L, Wang R. 2015. Bio-control of Salmonella Enteritidis in foods using bacteriophages. Viruses 7: 4836-4853. https://doi.org/10.3390/v7082847
  9. Zhang J, Li Z, Cao Z, Wang L, Li X, Li S, et al. 2015. Bacteriophages as antimicrobial agents against major pathogens in swine: a review. J. Anim. Sci. Biotechnol. 6: 39. https://doi.org/10.1186/s40104-015-0039-7
  10. Byeon HM, Vodyanoy VJ, Oh JH, Kwon JH, Park MK. 2015. Lytic phage-based magnetoelastic biosensors for on-site detection of methicillin-resistant Staphylococcus aureus on spinach leaves. J. Electrochem. Soc. 162: B230-B235. https://doi.org/10.1149/2.0681508jes
  11. Sillankorva SM, Oliveira H, Azeredo J. 2012. Bacteriophages and their role in food safety. Int. J. Microbiol. 2012: 863945.
  12. Singh A, Poshtiban S, Evoy S. 2013. Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors (Basel) 13: 1763-1786. https://doi.org/10.3390/s130201763
  13. Barlow M, Hall BG. 2002. Origin and evolution of the AmpC $\beta$-lactamases of Citrobacter freundii. Antimicrob. Agents Chemother. 46: 1190-1198. https://doi.org/10.1128/AAC.46.5.1190-1198.2002
  14. Cox N, Berrang M, Cason J. 2000. Salmonella penetration of egg shells and proliferation in broiler hatching eggs - a review. Poult. Sci. 79: 1571-1574. https://doi.org/10.1093/ps/79.11.1571
  15. Popoff MY, Bockemuhl J, Gheesling LL. 2003. Supplement 2001 (no. 45) to the Kauffmann-White scheme. Res. Microbiol. 154: 173-174. https://doi.org/10.1016/S0923-2508(03)00025-1
  16. Park MK, Oh JH, Chin BA. 2011. The effect of incubation temperature on the binding of Salmonella Typhimurium to phage-based magnetoelastic biosensors. Sens. Actuators B Chem. 160: 1427-1433. https://doi.org/10.1016/j.snb.2011.10.003
  17. Hungaro HM, Mendonca RCS, Gouvea DM, Vanetti MCD, de Oliveira Pinto CL. 2013. Use o f bacteriophages to reduce Salmonella in chicken skin in comparison with chemical agents. Food Res. Int. 52: 75-81. https://doi.org/10.1016/j.foodres.2013.02.032
  18. Ohl ME, Miller SI. 2001. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52: 259-274. https://doi.org/10.1146/annurev.med.52.1.259
  19. Bell C. 2002. Foodborne Pathogens. Hazards, Risk Analysis and Control. Woodhead Publishing, Boca Raton, FL.
  20. Currie A, MacDougall L, Aramini J, Gaulin C, Ahmed R, Isaacs S. 2005. Frozen chicken nuggets and strips and eggs are leading risk factors for Salmonella Heidelberg infections in Canada. Epidemiol. Infect. 133: 809-816. https://doi.org/10.1017/S0950268805004383
  21. Centers for Disease Control and Prevention (CDC). 2016. Reports of selected Salmonella outbreak investigations. Available from http://www.cdc.gov/salmonella/outbreaks.html.
  22. Yeh Y, Purushothaman P, Gupta N, Ragnone M, Verma SC, de Mello AS. 2017. Bacteriophage application on red meats and poultry: effects on Salmonella population in final ground products. Meat Sci. 127: 30-34. https://doi.org/10.1016/j.meatsci.2017.01.001
  23. Beuchat LR. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 4: 413-423. https://doi.org/10.1016/S1286-4579(02)01555-1
  24. Heaton JC, Jones K. 2008. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J. Appl. Microbiol. 104: 613-626. https://doi.org/10.1111/j.1365-2672.2007.03587.x
  25. Ye J, Kostrzynska M, Dunfield K, Warriner K. 2010. Control of Salmonella on sprouting mung bean and alfalfa seeds by using a biocontrol preparation based on antagonistic bacteria and lytic bacteriophages. J. Food Prot. 73: 9-17. https://doi.org/10.4315/0362-028X-73.1.9
  26. Sharma M. 2013. Lytic bacteriophages: potential interventions against enteric bacterial pathogens on produce. Bacteriophage 3: e25518. https://doi.org/10.4161/bact.25518
  27. Berends BR, Van Knapen F, Mossel DA, Burt SA, Snijders JM. 1998 Impact on human health of Salmonella spp. on pork in The Netherlands and the anticipated effects of some currently proposed control strategies. Int. J. Food Microbiol. 44: 219-229. https://doi.org/10.1016/S0168-1605(98)00121-4
  28. Hald T, Wegener HC. 1999. Quantitative assessment of the sources of human salmonellosis attributable to pork, pp. 200-205. In U.S. Swine Consortium, University of Illinois at Urbana-Champaign. Biomedical Communications Center (eds.), Proceedings of the 3rd International Symposium on the Epidemiology and Control of Salmonella in Pork, Washington DC, August 5-7, 1999. Iowa State University Digital Press, Ames, IA.
  29. C hen S, Z hao S, White DG, S chroeder C M, Lu R, Y ang H, et al. 2004. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl. Environ. Microbiol. 70: 1-7. https://doi.org/10.1128/AEM.70.1.1-7.2004
  30. Gebreyes WA, Thakur S. 2005. Multidrug-resistant Salmonella enterica serovar Muenchen from pigs and humans and potential interserovar transfer of antimicrobial resistance. Antimicrob. Agents Chemother. 49: 503-511. https://doi.org/10.1128/AAC.49.2.503-511.2005
  31. Akhtar M, Viazis S, Diez-Gonzalez F. 2014. Isolation, identification and characterization of lytic, wide host range bacteriophages from waste effluents against Salmonella enterica serovars. Food Control 38: 67-74. https://doi.org/10.1016/j.foodcont.2013.09.064
  32. Hudson J, Billington C, Carey-Smith G, Greening G. 2005. Bacteriophages as biocontrol agents in food. J. Food Prot. 68: 426-437. https://doi.org/10.4315/0362-028X-68.2.426
  33. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8: 317-327. https://doi.org/10.1038/nrmicro2315
  34. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, et al. 2001. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J. Food Prot. 64: 1116-1121. https://doi.org/10.4315/0362-028X-64.8.1116
  35. Greer GG. 2005. Bacteriophage control of foodborne bacteria. J. Food Prot. 68: 1102-1111. https://doi.org/10.4315/0362-028X-68.5.1102
  36. Sabouri S, Sepehrizadeh Z, Amirpour-Rostami S, Skurnik M. 2017. A mini review on the in vitro and in vivo experiments with anti-Escherichia coli O157:H7 phages as potential biocontrol and phage therapy agents. Int. J. Food Microbiol. 243: 52-57. https://doi.org/10.1016/j.ijfoodmicro.2016.12.004
  37. Abedon ST. 2008. Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press, Cambridge, UK.
  38. Wilhelm SW, Suttle CA. 1999. Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49: 781-788. https://doi.org/10.2307/1313569
  39. Little JW. 2005. Lysogeny, prophage induction, and lysogenic conversion, pp. 37-54. In Waldor M, Friedman D, Adhya S (eds.), Phages. ASM Press, Washington, DC.
  40. Grant AQ, Hashem F, Parveen S. 2016. Salmonella and Campylobacter: antimicrobial resistance and bacteriophage control in poultry. Food Microbiol. 53: 104-109. https://doi.org/10.1016/j.fm.2015.09.008
  41. Wilson WH, Carr NG, Mann NH. 1996. The effect of phosphage status on the kinetetis of cyanophage infection in the oceanic Cyanobacterium synechococcus sp. WH78031. J. Phycol. 32: 506-516. https://doi.org/10.1111/j.0022-3646.1996.00506.x
  42. Oliveira M, Vinas I, Colas P, Anguera M, Usall J, Abadias M. 2014. Effectiveness of a bacteriophage in reducing Listeria monocytogenes on fresh-cut fruits and fruit juices. Food Microbiol. 38: 137-142. https://doi.org/10.1016/j.fm.2013.08.018
  43. Haq IU, Chaudhry WN, Akhtar MN, Andleeb S, Qadri I. 2012. Bacteriophages and their implications on future biotechnology: a review. Virol. J. 9: 9. https://doi.org/10.1186/1743-422X-9-9
  44. Ackermann H-W. 2007. 5500 Phages examined in the electron microscope. Arch. Virol. 152: 227-243. https://doi.org/10.1007/s00705-006-0849-1
  45. Spricigo DA, Bardina C, Cortes P, Llagostera M. 2013. Use of a bacteriophage cocktail to control Salmonella in food and the food industry. Int. J. Food Microbiol. 165: 169-174. https://doi.org/10.1016/j.ijfoodmicro.2013.05.009
  46. Sukumaran AT, Nannapaneni R, Kiess A, Sharma CS. 2015. Reduction of Salmonella on chicken meat and chicken skin by combined or sequential application of lytic bacteriophage with chemical antimicrobials. Int. J. Food Microbiol. 207: 8-15. https://doi.org/10.1016/j.ijfoodmicro.2015.04.025
  47. Wang C, Yang J, Zhu X, Lu Y, Xue Y, Lu Z. 2017. Effects of Salmonella bacteriophage, nisin and potassium sorbate and their combination on safety and shelf life of fresh chilled pork. Food Control 73: 869-877. https://doi.org/10.1016/j.foodcont.2016.09.034
  48. Whichard JM, Sriranganathan N, Pierson FW. 2003. Suppression of Salmonella growth by wild-type and large-plaque variants of bacteriophage Felix O1 in liquid culture and on chicken frankfurters. J. Food Prot. 66: 220-225. https://doi.org/10.4315/0362-028X-66.2.220
  49. Modi R, Hirvi Y, Hill A, Griffiths M. 2001. Effect of phage on survival of Salmonella Enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J. Food Prot. 64: 927-933. https://doi.org/10.4315/0362-028X-64.7.927
  50. Zinno P, Devirgiliis C, Ercolini D, Ongeng D, Mauriello G. 2014. Bacteriophage P22 to challenge Salmonella in foods. Int. J. Food Microbiol. 191: 69-74. https://doi.org/10.1016/j.ijfoodmicro.2014.08.037
  51. Kocharunchitt C , Ross T, McNeil DL. 2009. Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int. J. Food Microbiol. 128: 453-459. https://doi.org/10.1016/j.ijfoodmicro.2008.10.014
  52. Higgins JP, Higgins S, Guenther K, Huff W, Donoghue A, Donoghue D, et al. 2005. Use of a specific bacteriophage treatment to reduce Salmonella in poultry products. Poult. Sci. 84: 1141-1145. https://doi.org/10.1093/ps/84.7.1141
  53. Oliveira M, Abadias M, Colas-Meda P, Usall J, Vinas I. 2015. Biopreservative methods to control the growth of foodborne pathogens on fresh-cut lettuce. Int. J. Food Microbiol. 214: 4-11. https://doi.org/10.1016/j.ijfoodmicro.2015.07.015
  54. Ye J, Kostrzynska M, Dunfield K, Warriner K. 2009. Evaluation of a biocontrol preparation consisting of Enterobacter asburiae JX1 and a lytic bacteriophage cocktail to suppress the growth of Salmonella Javiana associated with tomatoes. J. Food Prot. 72: 2284-2292. https://doi.org/10.4315/0362-028X-72.11.2284
  55. Magnone JP, Marek PJ, Sulakvelidze A, Senecal AG. 2013. Additive approach for inactivation of Escherichia coli O157:H7, Salmonella, and Shigella spp. on contaminated fresh fruits and vegetables using bacteriophage cocktail and produce wash. J. Food Prot. 76: 1336-1341. https://doi.org/10.4315/0362-028X.JFP-12-517
  56. Thung TY, Krishanthi Jayarukshi Kumari Premarathne JM, Chang WS, Loo YY, Chin YZ, Kuan CH, et al. 2017. Use of a lytic bacteriophage to control Salmonella Enteritidis in retail food. LWT Food Sci. Technol. 78: 222-225. https://doi.org/10.1016/j.lwt.2016.12.044
  57. Goode D, Allen VM, Barrow PA. 2003. Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69: 5032-5036. https://doi.org/10.1128/AEM.69.8.5032-5036.2003
  58. Guenther S, Herzig O, Fieseler L, Klumpp J, Loessner MJ. 2012. Biocontrol of Salmonella Typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int. J. Food Microbiol. 154: 66-72. https://doi.org/10.1016/j.ijfoodmicro.2011.12.023
  59. Goodridge LD, Bisha B. 2011. Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1: 130-137. https://doi.org/10.4161/bact.1.3.17629
  60. Williams HT. 2013. Phage-induced diversification improves host evolvability. BMC Evol. Biol. 13: 17. https://doi.org/10.1186/1471-2148-13-17
  61. Gill JJ, Hyman P. 2010. Phage choice, isolation, and preparation for phage therapy. Curr. Pharm. Biotechnol. 11: 2-14. https://doi.org/10.2174/138920110790725311
  62. Lone A, Anany H, Hakeem M, Aguis L, Avdjian A-C, Bouget M, et al. 2016. Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foods. Int. J. Food Microbiol. 217: 49-58. https://doi.org/10.1016/j.ijfoodmicro.2015.10.011
  63. Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA. 2006. Isolation and characterization of bacteriophages infecting Salmonella spp. FEMS Microbiol. Lett. 258: 182-186. https://doi.org/10.1111/j.1574-6968.2006.00217.x
  64. Kim SH, Park JH, Lee BK, Kwon HJ, Shin JH, Kim J, et al. 2012. Complete genome sequence of Salmonella bacteriophage SS3e. J. Virol. 86: 10253-10254. https://doi.org/10.1128/JVI.01550-12
  65. Augustine J, Louis L, Varghese SM, Bhat SG, Kishore A. 2013. Isolation and partial characterization of ${\Phi}SP-1$, a Salmonella specific lytic phage from intestinal content of broiler chicken. J. Basic Microbiol. 53: 111-120. https://doi.org/10.1002/jobm.201100319
  66. Santos SB, Kropinski AM, Ceyssens PJ, Ackermann HW, Villegas A, Lavigne R, et al. 2011. Genomic and proteomic characterization of the broad-host-range Salmonella phage PVP-SE1: creation of a new phage genus. J. Virol. 85: 11265-11273. https://doi.org/10.1128/JVI.01769-10
  67. Tiwari BR, Kim S, Kim J. 2013. A virulent Salmonella enterica serovar Enteritidis phage SE2 with a strong bacteriolytic activity of planktonic and biofilmed cells. J. Bacteriol. Virol. 43: 186-194. https://doi.org/10.4167/jbv.2013.43.3.186
  68. Turner D, Hezwani M, Nelson S, Salisbury V, Reynolds D. 2012. Characterization of the Salmonella bacteriophage vB_SenS-Ent1. J. Gen. Virol. 93: 2046-2056. https://doi.org/10.1099/vir.0.043331-0
  69. De Lappe N, Doran G, O'Connor J, O'Hare C, Cormican M. 2009. Characterization of bacteriophages used in the Salmonella enterica serovar Enteritidis phage-typing scheme. J. Med. Microbiol. 58: 86-93. https://doi.org/10.1099/jmm.0.000034-0
  70. Bao H, Zhang H, Wang R. 2011. Isolation and characterization of bacteriophages of Salmonella enterica serovar Pullorum. Poult. Sci. 90: 2370-2377. https://doi.org/10.3382/ps.2011-01496
  71. Park M, Lee JH, Shin H, Kim M, Choi J, Kang DH, et al. 2012. Characterization and comparative genomic analysis of a novel bacteriophage, SFP10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157:H7. Appl. Environ. Microbiol. 78: 58-69. https://doi.org/10.1128/AEM.06231-11
  72. Lee JH, Shin H, Kim H, Ryu S. 2011. Complete genome sequence of Salmonella bacteriophage SPN3US. J. Virol. 85: 13470-13471. https://doi.org/10.1128/JVI.06344-11
  73. Pickard D, Thomson NR, Baker S, Wain J, Pardo M, Goulding D, et al. 2008. Molecular characterization of the Salmonella enterica serovar Typhi Vi-typing bacteriophage E1. J. Bacteriol. 190: 2580-2587. https://doi.org/10.1128/JB.01654-07
  74. Bunny K, Liu J, Roth J. 2002. Phenotypes of lexA mutations in Salmonella enterica: evidence for a lethal lexA null phenotype due to the Fels-2 prophage. J. Bacteriol. 184: 6235-6249. https://doi.org/10.1128/JB.184.22.6235-6249.2002
  75. Shin H, Lee J-H, Yoon H, Kang D-H, Ryu S. 2014. Genomic investigation of lysogen formation and host lysis systems of the Salmonella temperate bacteriophage SPN9CC. Appl. Environ. Microbiol. 80: 374-384. https://doi.org/10.1128/AEM.02279-13
  76. Wang C, Chen Q, Zhang C, Yang J, Lu Z, Lu F, et al. 2017. Characterization of a broad host-spectrum virulent Salmonella bacteriophage fmb-p1 and its application on duck meat. Virus Res. 236: 14-23. https://doi.org/10.1016/j.virusres.2017.05.001
  77. Kerketta P, Agarwal R, Rawat M, Jain L, Kumar PP, Dhanze H, et al. Isolation and characterization of lytic bacteriophage (${\phi}STIz1$) against Salmonella enterica serovars Typhimurium. J. Pure Appl. Microbiol. 8: 4719-4726
  78. Kim S. 2013. Isolation and characterization of bacteriophage SSU5 specific for Salmonella enterica serovar Typhimurium rough strain. Master's Thesis. 52 pages. Seoul National University, Korea.
  79. Pereira C, Moreirinha C, Lewicka M, Almeida P, Clemente C, Cunha A, et al. 2016. Bacteriophages with potential to inactivate Salmonella Typhimurium: use of single phage suspensions and phage cocktails. Virus Res. 220: 179-192. https://doi.org/10.1016/j.virusres.2016.04.020
  80. Joshi A, Siddiqi J, Rao G, Chakravorty M. 1982. MB78, a virulent bacteriophage of Salmonella typhimurium. J. Virol. 41: 1038-1043.
  81. Hungaro HM, Mendonca RCS, Gouvea DM, Vanetti MCD, de Oliveira Pinto CL. 2013. Use of bacteriophages to reduce Salmonella in chicken skin in comparison with chemical agents. Food Res. Int. 52: 75-81. https://doi.org/10.1016/j.foodres.2013.02.032
  82. Santos R, Avena M, Gumafelix REJ, Mamuric GAA, Pastoral AKD, Papa DMD. 2014. The first report of a Salmonella enterica serovar Havana phage and its lytic activity at storage temperature of processed chicken. Acta Manilana 62: 35-40.
  83. Bigwood T, Hudson JA, Billington C, Carey-Smith GV, Heinemann JA. 2008. Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiol. 25: 400-406. https://doi.org/10.1016/j.fm.2007.11.003
  84. Hooton SP, Atterbury RJ, Connerton IF. 2011. Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin. Int. J. Food Microbiol. 151: 157-163. https://doi.org/10.1016/j.ijfoodmicro.2011.08.015
  85. Lakshmanan RS. 2008. Phage-based magnetoelastic sensor for the detection of Salmonella Typhimurium. Ph.D. Thesis. 150 pages. Auburn University, USA.

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