Bacteriophages with potential to inactivate Salmonella Typhimurium: Use of single phage suspensions and phage cocktails

Virus Research

Volumn 220, Issue , 2016, Pages 179-192

  Pereira, Carla ^a   Moreirinha, Catarina ^a   Lewicka, Magdalena ^b   Almeida, Paulo ^b   Clemente, Carla ^b   Cunha, Ângela ^a   Delgadillo, Ivonne ^a   Romalde, Jésus L ^c   Nunes, Maria L ^d   Almeida, Adelaide ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b Madan Parque   (Portugal)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

Bacterial phage inactivation; Phage cocktails; Phenotypic resistance; Salmonella Typhimurium; Salmonellosis

Indexed keywords

AMIDE; CARBOHYDRATE; PHOSPHATE; PROTEIN; SEA WATER;

ADSORPTION; ARTICLE; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM MUTANT; BIVALVE; CONTROLLED STUDY; HOST RANGE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; SIPHOVIRIDAE; SURVIVAL; SUSPENSION; ANIMAL; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; PATHOGENICITY; SALMONELLA PHAGE; VIROLOGY;

ANIMALS; BIVALVIA; HOST SPECIFICITY; MICROBIAL VIABILITY; MUTATION; SALMONELLA PHAGES; SALMONELLA TYPHIMURIUM; SEAWATER; SIPHOVIRIDAE;

EID: 84969246749     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2016.04.020     Document Type: Article

References (74)

1. Abedon S., Culler R.R. Optimizing bacteriophage plaque fecundity. J. Theor. Biol. 2007, 249:582-592.
2. Abedon S.T. Lysis from without. Bacteriophage 2011, 1:46-49.
3. Adams M.H. Bacteriophages 1959, John Wiley and Sons Inc, New York.
4. Allison G.E., Klaenhammer T.R. Phage resistance mechanisms in lactic acid bacteria. Int. Dairy J. 1998, 8:207-226.
5. Almeida M.A., Alcantara F. Bacterial colonization of seston particles in brackish waters (Ria de Aveiro, Portugal). Mar. Ecol. Prog. Ser. 1992, 89:165-173.
6. Almeida M.A., Cunha M.A., Alcântara F. Seasonal change in the proportion of bacterial and phytoplankton production along a salinity gradient in a shallow estuary. Hydrobiologia 2002, 475/476:251-262.
7. Almeida A., Cunha Â., Gomes N.C.M., Alves E., Costa L., Faustino M.A.F. Phage therapy and photodynamic therapy: low environmental impact approaches to inactivate microorganisms in fish farming plants. Mar. Drugs 2009, 7:268-313.
8. Alves E., Carvalho C.M.B., Tomé J.P.C., Faustino M.A.F., Neves M.G.P.M.S., Tomé A.C., Cavaleiro J.A.S., Cunha A., Mendo S., Almeida A. Photodynamic inactivation of recombinant bioluminescent Escherichia coli by cationic porphyrins under artificial and solar irradiation. J. Ind. Microbiol. Biotechnol. 2008, 35:1447-1454.
9. Aziz R.K., Bartels D., Best A.A., DeJongh M., Disz T., Edwards R.A., Formsma K., Gerdes S., Glass E.M., Kubal M., Meyer F., Olsen G.J., Olson R., Osterman A.L., Overbeek R.A., McNeil L.K., Paarmann D., Paczian T., Parrello B., Pusch G.D., Reich C., Stevens R., Vassieva O., Vonstein V., Wilke A., Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75.
10. Barrangou R., Fremaux C., Deveau H., Richards M., Patrick Boyaval Moineau S., Romero D., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315(80):1709-1712.
11. Barros A. Contribution à la Sélection et la Comparaison de Variables Caractéristiques 1999, Institut National Agronomique Paris-Grignon, Paris, France.
12. Barth A. Infrared spectroscopy of proteins. Biochim. Biophys. Acta 2007, 1767:1073-1101.
13. Brands D.A., Inman A.E., Gerba C.P., Maré C.J., Billington S.J., Saif L.A., Levine J.F., Joens L.A. Prevalence of Salmonella spp. in oysters in the United States. Appl. Environ. Microbiol. 2005, 71:893-897.
14. Bueno E., García P., Martínez B., Rodríguez A. International Journal of Food Microbiology phage inactivation of Staphylococcus aureus in fresh and hard- type cheeses. Int. J. Food Microbiol. 2012, 158:23-27.
15. Bull J.J., Vegge C.S., Schmerer M., Chaudhry W.N., Levin B.R. Phenotypic resistance and the dynamics of bacterial escape from phage control. PLoS One 2014, 9:e94690.
16. Butt A.A., Aldridge K.E., Sanders C.V. Infections related to the ingestion of seafood Part I: viral and bacterial infections. Lancet Infect. Dis. 2004, 4:201-212.
17. Cairns B.J., Timms A.R., Jansen V.A.A., Connerton I.F., Payne R.J.H. Quantitative models of in vitro bacteriophage-host dynamics and their application to phage therapy. PLoS Pathog. 2009, 5:1-10.
18. Carter C.D., Parks A., Abuladze T., Li M., Woolston J., Magnone J., Senecal A., Kropinski A.M., Sulakvelidze A. Bacteriophage cocktail significantly reduces Escherichia coli O157: H7 contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage 2012, 2:178-185.
19. Chan B.K., Abedon S.T., Loc- carrillo C. Phage cocktails and the future of phage therapy. Futur. Med. 2013, 8:769-783.
20. Crothers-Stomps C., Høj L., Bourne D.G., Hall M.R., Owens L. Isolation of lytic bacteriophage against Vibrio harveyi. J. Appl. Microbiol. 2010, 108:1744-1750.
21. FAO, 2004. Assessment and management of seafood safety and quality, FAO Fisheries technical paper. Rome.
22. FAO, 2008. Bivalve depuration: fundamental and practical aspects. FAO Fisheries technical paper, Rome, pp. 1-161.
23. Filippov A.A., Sergueev K.V., He Y., Huang X.-Z., Gnade B.T., Mueller A.J., Fernandez-Prada C.M., Nikolich M.P. Bacteriophage-resistant mutants in Yersinia pestis: identification of phage receptors and attenuation for mice. PLoS One 2011, 6:e25486.
24. Finstad S., O'Bryan C.A., Marcy J.A., Crandall P.G., Ricke S.C. Salmonella and broiler processing in the United States: relationship to foodborne salmonellosis. Food Res. Int. 2012, 45:789-794.
25. Flynn G.O., Ross R.P., Fitzgerald G.F., Coffey A. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157: H7 evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157: H7. Appl. Environ. Microbiol. 2004, 70:3417-3424.
26. Gill J.J., Hyman P. Phage choice, isolation, and preparation for phage therapy. Curr. Pharm. Biotechnol. 2010, 11(January (1)):2-14.
27. Grimont P.A.D., Weill F.-X. Antigenic formulas of the Salmonella serovars 7th revision. Res. Salmonella. Inst. Pasteur 1997, 9:1-166. WHO Collab. Cent. Ref.
28. Hawkins C., Harper D., Burch D., Anggard E., Soothill J. Topical treatment of Pseudomonas aeruginosa otitis of dogs with a bacteriophage mixture: a before/after clinical trial. Vet. Microbiol. 2010, 146:309-313.
29. Heller K.J. Molecular interaction between bacteriophage and the gram negative cell envelope. Arch. Microbiol. 1992, 158:235-248.
30. Hooton S.P.T., Atterbury R.J., Connerton I.F. Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin. Int. J. Food Microbiol. 2011, 151:157-163.
31. Huss H.H., Reilly A., Karim Ben Embarek P. Prevention and control of hazards in seafood. Food Control 2000, 11:149-156.
32. Kanayama A., Yahata Y., Arima Y., Takahashi T., Saitoh T., Kanou K., Kawabata K., Sunagawa T., Matsui T., Oishi K. Enterohemorrhagic Escherichia coli outbreaks related to childcare facilities in Japan, 2010-2013. BMC Infect. Dis. 2015, 15:539.
33. Karunasagar I., Shivu M.M., Girisha S.K., Krohne G., Karunasagar I. Biocontrol of pathogens in shrimp hatcheries using bacteriophages. Aquaculture 2007, 268:288-292.
34. Kudva I.T., Jelacic S., Tarr P.I., Hovde C.J., Youderian P. Biocontrol of Escherichia coli O157 with biocontrol of Escherichia coli O157 with O157-Specific bacteriophages. Appl. Environ. Microbiol. 1999, 65:3767-3773.
35. Kunisaki H., Tanji Y. Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli O157: H7 in anaerobic continuous culture. Appl. Genet. Mol. Biotechnol. 2010, 85:1533-1540.
36. Kutter E. Phage host range and efficiency of plating. Bacteriophages: Methods and Protocols 2009, 141-149. Humana Press. M.R.J. Clokie, A.M. Kropinski (Eds.).
37. Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8:317-327.
38. Levin B.R., Bull J.J. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2004, 2:20-24.
39. Lim T., Kim M., Lee D., Lee Y., Park J., Youn H., Lee H., Yang S., Cho Y., Lee J., Park S., Choi I., Song C. Use of bacteriophage for biological control of Salmonella Enteritidis infection in chicken. Res. Vet. Sci. 2012, 93:1173-1178.
40. Louvado A., Coelho F.J.R.C., Domingues P., Santos A.L., Gomes N.C.M., Almeida A., Cunha Â. Isolation of surfactant-resistant pseudomonads from the estuarine surface microlayer. J. Microbiol. Biotechnol. 2012, 22:283-291.
41. Martínez O., Rodríguez-Calleja J.M., Santos J.A., Otero A., García-López M.L. Foodborne and indicator bacteria in farmed molluscan shellfish before and after depuration. J. Food Prot. 2009, 72:1443-1449.
42. Mateus L., Costa L., Silva Y.J., Pereira C., Cunha A., Almeida A. Efficiency of phage cocktails in the inactivation of Vibrio in aquaculture. Aquaculture 2014, 424-425:167-173.
43. Mendes C. Importance of Lisogeny in the Marine Environment (ThesisMsc) 2009, Department of Biology, University of Aveiro.
44. Merabishvili M., Pirnay J., Verbeken G., Chanishvili N., Tediashvili M., Lashkhi N., Glonti T., Krylov V., Mast J., Parys L., Van Lavigne R., Volckaert G., Mattheus W., Verween G., Corte P., De Rose T., Jennes S., Zizi M., Vos D., De Vaneechoutte M. Quality-controlled small-scale production of a well- defined bacteriophage cocktail for use in human clinical trials. PLoS One 2009, 4:e4944.
45. Mizoguchi K., Morita M., Fischer C.R., Yoichi M., Tanji Y., Unno H. Coevolution of bacteriophage PP01 and Escherichia coli O157: H7 in continuous culture. Appl. Environ. Microbiol. 2003, 69:170-176.
46. Mirzaei M., Nilsson A.S. 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 2015, 10:e0118557.
47. Moreirinha C., Nunes A., Barros A., Almeida A., Delgadillo I. Evaluation of the potential of mid-infrared spectroscopy to assess the microbiological quality of Ham. J. Food Saf. 2015, 35:270-275.
48. Movasaghi Z., Rehman S., Rehman I. Fourier transform infrared (FTIR) spectroscopy of biological tissues fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl. Spectrosc. Rev. 2008, 43:134-179.
49. Muniain-Mujika I., Calvo M., Lucena F., Girones R. Comparative analysis of viral pathogens and potential indicators in shellfish. Int. J. Food Microbiol. 2003, 83:75-85.
50. Nakai T. Application of bacteriophages for control of infectious diseases in aquaculture. Bacteriophages in the Control of Food and Waterborne Pathogens 2010, 257-272. ASM Press, Washington, USA. P. Sabour, M. Griffiths (Eds.).
51. O'Flynn G., Coffey A., Fitzgerald G., Ross R. The newly isolated lytic bacteriophages st104a and st104b are highly virulent against Salmonella enterica. J. Appl. Microbiol. 2006, 101:251-259.
52. Park S., Nakai T. Bacteriophage control of Pseudomonas plecoglossicida infection in ayu. Dis. Aquat. Organ. 2003, 53:33-39.
53. Pereira C., Silva Y.J., Santos A.L., Cunha Â., Gomes N.C.M., Almeida A. Bacteriophages with potential for inactivation of fish pathogenic bacteria: survival, host specificity and effect on bacterial community structure. Mar. Drugs 2011, 9:2236-2255.
54. Pereira C., Santos L., Silva A.P., Silva Y.J., Cunha A., Romalde J.L., Nunes M.L., Almeida A. Seasonal variation of bacterial communities in shellfish harvesting waters: preliminary study before applying phage therapy. Mar. Pollut. Bull. 2015, 90:68-77.
55. Pereira S., Pereira C., Santos L., Klumpp J., Almeida A. Potential of phage cocktails in the inactivation of Enterobacter cloacae-an in vitro study in a buffer solution and in urine samples. Virus Res. 2016, 211:199-208.
56. Potasman I., Paz A., Odeh M. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis. 2002, 35:921-928.
57. Robertson L.J. The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. Int. J. Food Microbiol. 2007, 120:201-216.
58. Rong R., Lin H., Wang J., Khan M.N., Li M., Naseem M., Li M., Khan M.N., Li M. Reductions of Vibrio parahaemolyticus in oysters after bacteriophage application during depuration. Aquaculture 2014, 418-419:171-176.
59. Sandeep K. Bacteriophage precision drug against bacterial infections. Curr. Sci. 2006, 90:631-633.
60. Santos A.L., Moreirinha C., Lopes D., Esteves A.C., Henriques I., Almeida A., Rosa M., Domingues M., Delgadillo I. Effects of UV radiation on the lipids and proteins of bacteria studied by mid-infrared spectroscopy. Environ. Sci. Technol. 2013, 47:6306-6315.
61. Scott A.E., Timms A.R., Connerton P.L., Carrillo C.L., Radzum K.A., Connerton I.F. Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathog. 2007, 3:e119.
62. Silva Y.J., Costa L., Pereira C., Mateus C., Cunha Â., Calado R., Gomes N.C.M., Pardo M.A., Hernandez I., Almeida A. Phage therapy as an approach to prevent Vibrio anguillarum infections in fish larvae production. PLoS One 2014, 9:e114197.
63. Silva Y.J., Moreirinha C., Pereira C., Costa L., Rocha R.J.M., Cunha Â., Gomes N.C.M., Calado R., Almeida A. Biological control of Aeromonas salmonicida infection in juvenile Senegalese sole (Solea senegalensis) with Phage AS-A. Aquaculture 2016, 450:225-233.
64. Silva-aciares F., Moraga D., Auffret M., Tanguy A., Riquelme C. Transcriptomic and cellular response to bacterial challenge (pathogenic Vibrio parahaemolyticus) in farmed juvenile Haliotis rufescens fed with or without probiotic diet. J. Invertebr. Pathol. 2013, 113:163-176.
65. Skurnik M., Strauch E. Phage therapy: facts and fiction. Int. J. Med. Microbiol. 2006, 296:5-14.
66. Stuer-Lauridsen B., Janzen T., Schnabl J., Johansen E. Identification of the host determinant of two prolate- headed phages infecting Lactococcus lactis. Virology 2003, 309:10-17.
67. Sulakvelidze A., Alavidze Z., Glenn J., Morris J. Bacteriophage therapy. Antimicrob. Agents Chemother. 2001, 45:649.
68. Tanji Y., Shimada T., Yoichi M., Miyanaga K., Hori K., Unno H. Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl. Microbiol. Biotechnol. 2004, 64:270-274.
69. Tanji Y., Shimada T., Fukudomi H., Miyanaga K., Nakai Y., Unno H. Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J. Biosci. Bioeng. 2005, 100:280-287.
70. Tomat D., Mercanti D., Balagu C., Quiberoni A. Phage biocontrol of enteropathogenic and shiga toxin- producing Escherichia coli during milk fermentation. Lett. Appl. Microbiol. 2013, 57:3-10.
71. Viazis S., Akhtar M., Feirtag J., Diez-gonzalez F. Reduction of Escherichia coli O157: H7 viability on hard surfaces by treatment with a bacteriophage mixture. Int. J. Food Microbiol. 2011, 145:37-42.
72. Vieira A., Silva Y.J., Cunha Â., Gomes N.C.M., Ackermann H.-W., Almeida A. Phage therapy to control multidrug-resistant Pseudomonas aeruginosa skin infections: in vitro and ex vivo experiments. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31:3241-3249.
73. Vinod M.G., Shivu M.M., Umesha K.R., Rajeeva B.C., Krohne G. Isolation of Vibrio harveyi bacteriophage with a potential for biocontrol of luminous vibriosis in hatchery environments. Aquaculture 2006, 255:117-124.
74. Wagner P.L., Waldor M.K. Bacteriophage control of bacterial virulence. Infect. Immun. 2002, 70:3985-3993.