Salmonella pp 177-211 | Cite as

Salmonella Typhimurium Phage Typing for Pathogens

  • Wolfgang Rabsch
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 394)

Abstract

Phage typing provides a rapid, accurate, and cheap method of investigating Salmonella strains for epidemiological use. Salmonella strains within a particular serovar may be differentiated into a number of phage types by their pattern of susceptibility to lysis by a set of phages with different specificity. Characterization based on the pattern of phage lysis of wild strains isolated from different patients, carriers, or other sources is valuable in epidemiological study. The phages must have well-defined propagation strains that allow reproducible discrimination between different Salmonella Typhimurium strains. Different schemes have been developed for this serovar in different countries. The Felix/Callow (England) and Lilleengen typing systems (Sweden) used for laboratory-based epidemiological analysis were helpful for control of salmonellosis. More recently, the extended phage-typing system of Anderson (England) that distinguishes more than 300 definitive phage types (DTs) has been used worldwide in Europe, the United States, and Australia. The use of this method for decades show us that some phage types (DT204 in the 1970s and DT104 in the 1990s) have a broad host range and are distributed worldwide, other phage types such as DT2 or DT99 are frequently associated with disease in pigeons, indicative of a narrow host range.

Key Words

Bacteriophages definitive phage type (DT) Salmonella epidemiological tool lysogenic conversion phage adsorption super infection exclusion 
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References

  1. 1.
    Mead, P. S., Slutsker, L., Dietz, V., et al. (1999) Food-related illness and death in the United States. Emerg. Infect. Dis. 5, 607–625.CrossRefPubMedGoogle Scholar
  2. 2.
    Chalker, R. B. and Blaser, M. J. (1988) A review of human Salmonellosis: III. Magnitude of Salmonella infection in the United States. Rev. Infect. Dis. 10, 111–124.PubMedGoogle Scholar
  3. 3.
    Voetsch, A. C., van Gilder, T. J., Angulo, F. J., et al. (2004) FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States — Emerging Infections Program FoodNet Working Group. Clin. Infect. Dis. 15,38 Suppl. 3, S127–134.CrossRefGoogle Scholar
  4. 4.
    Galbraith, N. S. (1961) Studies of human salmonelloses in relation to infection in animals. Vet. Rec. 73, 1296–1303.PubMedGoogle Scholar
  5. 5.
    Rabsch, W., Altier, C., Tschäpe, H., and Bäumler, A. J. (2003) Foodborne Salmonella infections, in Microbial Food Safety in Animal Agriculture. Current Topics (Torrence, M. E. and Isaacson, R. E., eds.), Iowa State Press, pp. 97–107.Google Scholar
  6. 6.
    CDC (1996) Salmonella surveillance: annual tabulation summary, 1993–1995 US Department of Health and Human Services. CDC, Atlanta.Google Scholar
  7. 7.
    Sonnenschein, C. (1928) Bakteriendiagnose mit Bakteriophagen. Deutsche Medizinische Wochenschr. 25, 1–4.Google Scholar
  8. 8.
    Marcuse, K. (1934) Über Typhusdiagnostik mit spezifischen Bakteriophagen (nach Sonnenschein). Zentralbl. Bakteriol. Abt.i 131, 206–211.Google Scholar
  9. 9.
    Cragie, J. and Yen, C. H. (1938a) The demonstration of types of B. ityphosus by means of preparations of Type II Vi-phage. 1. Can. Public Health J. 29, 448–463.Google Scholar
  10. 10.
    Cragie, J. and Yen, C. H. (1938b) The demonstration of types of B. typhosus by means of preparations of Type II Vi-phage. 2. Can. Public Health J. 29, 484–496.Google Scholar
  11. 11.
    Craigie, J. and Felix, A. (1947) Typing of typhoid bacilli with Vi bacteriophage. Lancet i, 823–827.CrossRefGoogle Scholar
  12. 12.
    Lilleengen, K. (1948) Typing of Salmonella Typhimurium by means of bacteriophage. Acta Pathol. Microbiol. Scand. Suppl. 77, 1–39.Google Scholar
  13. 13.
    Ward, L. R., de Sa, J. D., and Rowe, B. (1987) A phage-typing scheme for Salmonella Enteritidis. Epidemiol. Infect. 99, 291–294.CrossRefPubMedGoogle Scholar
  14. 14.
    Rabsch, W., Prager, R., Koch, J., et al. (2005) Molecular epidemiology of Salmonella enterica serovar Agona: characterization of a diffuse outbreak caused by aniseed-fennel-caraway infusion. Epidemiol. Infect. 133, 837–844.CrossRefPubMedGoogle Scholar
  15. 15.
    Fisher, I. S. and Enter-net participants (2004) Dramatic shift in the epidemiology of Salmonella enterica serotype Enteritidis phage types in Western Europe, 1998–2003 — results from the Enter-net international Salmonella database. Eur. Surveill. 9, 43–45.Google Scholar
  16. 16.
    Helm, R. A., Porwollik, S., Stanley, A. E., et al. (2004) Pigeon-associated strains of Salmonella enterica serovar Typhimurium phage type DT2 have genomic rearrangements at rRNA operons. Infect. Immun. 72, 7338–7341.CrossRefPubMedGoogle Scholar
  17. 17.
    Rabsch, W., Andrews, H. L., Kingsley, R. A., et al. (2002) Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect. Immun. 70, 2249–2255.CrossRefPubMedGoogle Scholar
  18. 18.
    Bratbak, G., Heldal, M., Norland, S., and Thingstad, T. F. (1990) Viruses as partners in spring bloom microbial trophodynamics. Appl. Environ. Microbiol. 56, 1400–1405.PubMedGoogle Scholar
  19. 19.
    Procter, L. M., Okubo, A., and Fuhrmann, J. A. (1993) Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microb. Ecol. 25, 161–182.Google Scholar
  20. 20.
    Thingstad, T. F. (2000) Elements of a theory for the mechanisms controlling abundance diversity and biogeochemical role of lytic bacterial virus in aquatic systems. Limnol. Oceanogr. 45, 1320–1914.CrossRefGoogle Scholar
  21. 21.
    Schicklmaier, P. and Schmieger, H. (1995) Frequency of generalized transducing phages in natural isolates of the Salmonella Typhimurium complex. Appl. Environ. Microbiol. 61, 1637–1640.PubMedGoogle Scholar
  22. 22.
    Zinder, N. D. and Lederberg, J. (1952) Genetic exchange in Salmonella. J. Bacteriol. 64, 679–699.CrossRefPubMedGoogle Scholar
  23. 23.
    Kuo, T.-T. and Stocker, B. A. D. (1978) ES18, a general transducing phage for smooth and non-smooth Salmonella Typhimuirum. Virology 42, 621–632.CrossRefGoogle Scholar
  24. 24.
    Sanderson, K. E. (1972) Linkage map of Salmonella Typhimurium, edition IV. Bacteriol. Rev. 36, 558–586.PubMedGoogle Scholar
  25. 25.
    Schmieger, H. (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119, 75–88CrossRefPubMedGoogle Scholar
  26. 26.
    Mirold, S., Rabsch, W., Rohde, M., et al. (1999) Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella Typhimurium strain. Proc. Natl. Acad. Sci. USA 96, 9845–9850.CrossRefPubMedGoogle Scholar
  27. 27.
    Hopkins, K. L. and Threlfall, E. J. (2004) Frequency and polymorphism of sopE in isolates of Salmonella enterica belonging to the ten most prevalent serotypes in England and Wales. J. Med. Microbiol. 53, 539–543.CrossRefPubMedGoogle Scholar
  28. 28.
    Wray, C., Beedell, Y. E., and McLaren, I. M. (1991) A survey of antimicrobial resistance in salmonellae isolated from animals in England and Wales during 1984–1987. Br. Vet. J. 147, 356–369.PubMedGoogle Scholar
  29. 29.
    Threlfall, E. J., Ward, L. R., and Rowe, B. (1978) Spread of multiresistant strains of Salmonella Typhimurium phage types 204 and 193 in Britain. Br. Med. J. 2, 997.CrossRefPubMedGoogle Scholar
  30. 30.
    Threlfall, E. J., Frost, J. A., Ward, L. R., and Rowe, B. (1990) Plasmid profile typing can be used to subdivide phage-type 49 of Salmonella Typhimurium in outbreak investigations. Epidemiol. Infect. 104, 243–251.CrossRefPubMedGoogle Scholar
  31. 31.
    Kühn, H., Rabsch, W., Tschäpe, H., and Tietze, E. (1982) Characterization and epidemiology of a Salmonella Typhimurium epidemic strain. Z. Ärztl. Fortbild. (Jena) 70, 607–610.Google Scholar
  32. 32.
    Ehrbar, K., Mirold, S., Friebel, A., Stender, S., and Hardt, W. D. (2002) Characterization of effector proteins translocated via the SPI1 type III secretion system of Salmonella Typhimurium. Int. J. Med. Microbiol. 291, 479–485.CrossRefPubMedGoogle Scholar
  33. 33.
    Fang, F. C., DeGroote, M. A., Foster, J. W., et al. (1999) Virulent Salmonella Typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl. Acad. Sci. USA 96, 7502–7507.CrossRefPubMedGoogle Scholar
  34. 34.
    Figueroa-Bossi, N., Uzzau, S., Maloriol, D., and Bossi, L. (2001) Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol. Microbiol. 39, 260–272.CrossRefPubMedGoogle Scholar
  35. 35.
    Hardt, W. D., Urlaub, H., and Galan, J. E. (1998) A substrate of the centrisome 63 type III protein secretion system of Salmonella Typhimurium is encoded by a cryptic bacteriophage. Proc. Natl. Acad. Sci. USA 95, 2574–2579.CrossRefPubMedGoogle Scholar
  36. 36.
    Miao, E. A., Scherer, A., Tsolis, R. M., et al. (1999) Salmonella Typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type secretion systems. Mol. Microbiol. 34, 850–864.CrossRefPubMedGoogle Scholar
  37. 37.
    Brussow H., Canchaya C., and Hardt W. D. (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602.CrossRefPubMedGoogle Scholar
  38. 38.
    Stone, R. (2002) Bacteriophage therapy: Stalin’s forgotten cure, Science 298, 728–731.CrossRefPubMedGoogle Scholar
  39. 39.
    Weber-Dabrowska, B., Mulczyk, M., and Gorski, A. (2000) Bacteriophage therapy of bacterial infections: an update of our institute’s experience. Arch. Immunol. Ther. Exp. (Warsz), 48, 547–551.Google Scholar
  40. 40.
    Berchieri, A. Jr., Lovell, M. A., and Barrow, P. A. (1991) The activity in the chicken alimentary tract of bacteriophages lytic for Salmonella Typhimurium. Res. Microbiol. 142, 541–549.CrossRefPubMedGoogle Scholar
  41. 41.
    Rabsch, W., Wiley, G., Najar, F. Z., Kaserer, W., Schuerch, D. W., Klebba, J. E., Roe, B. A., Gomez, J. A. L., Schallmey, M., Newton, S. M. C., and Klebba, P. E. (2007) FepA-and TonB-dependent Bacteriophage H8: Receptor Binding and Genomic Sequence. J. Bact. (in press).Google Scholar
  42. 42.
    Chanishvili, N., Chanishvili, T., Tediashvili, M., and Barrow, P. A. (2001) Review: phages and their application against drug-resistant bacteria. J. Chem. Technol. Biotechnol. 76, 689–699.CrossRefGoogle Scholar
  43. 43.
    Hänggi, B. J. (2004) Die Phagentherapie und das Problem ihrer Verwirklichung — ein Beitrag zur gegenwärtigen Rückbesinnung auf ein medizinhistorisches Phänomen. Inauguraldissertation der Universität Bern, Schweiz.Google Scholar
  44. 44.
    Goode, D., Allen, V. M., and Barrow, P. A. (2003) Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl. Environ. Microbiol. 69, 5032–5036.CrossRefPubMedGoogle Scholar
  45. 45.
    Leverentz, B., Conway, W. S., Alavidze, Z., 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.PubMedGoogle Scholar
  46. 46.
    Kallings, L. O. and Laurell, A.-B. (1957) Relation between phage types and fermentation types of Salmonella Typhimurium. Acta Pathol. Microbiol. Scand. 40, 328–342.PubMedGoogle Scholar
  47. 47.
    Lundbeck, H., Plazikowski, U., and Silverstolpe, L. (1955) The Swedish Salmonella outbreak of 1953. J. Appl. Bacteriol. 18, 535–548.Google Scholar
  48. 48.
    Kallings, L. O., Laurell, A.-B., and Zetterberg, B. (1959) An outbreak due to Salmonella typhimurium in veal with special reference to phage and fermentation typing. Acta Pathol. Microbiol. Scand. 45, 347–356.CrossRefPubMedGoogle Scholar
  49. 49.
    Callow, B. R. (1959) A new phage-typing scheme for Salmonella Typhimurium. J. Hyg., Camb. 57, 346–359.CrossRefGoogle Scholar
  50. 50.
    Anderson, E. S., Ward, L. R., Saxe, M. J., and de Sa, J. D. (1977) Bacteriophagetyping designations of Salmonella Typhimurium. J. Hyg. (Lond). 78, 297–300.CrossRefGoogle Scholar
  51. 51.
    Kühn, H., Falta, R., and Rische, H. (1973) Salmonella Typhimurium, in Lysotypie und andere spezielle epidemiologische Laboratoriumsmethoden (Rische, H., ed.), VEB Gustav Fischer Verlag Jena, pp. 101–139.Google Scholar
  52. 52.
    Kohler, B., Vogel, K., Kuhn, H., et al. (1979) Epizootiology of Salmonella Typhimurium infection in chickens. Arch. Exp. Veterinarmed. 33, 281–298.PubMedGoogle Scholar
  53. 53.
    Hasenson, L., Gericke, B., Liesegang, A., et al. (1995) Epidemiological and microbiological studies on salmonellosis in Russia. Zentralbl. Hyg. Umweltmed. 198, 97–116.PubMedGoogle Scholar
  54. 54.
    Rabsch, W., Tschäpe, H., and Kühn, H. (1985) Phage type changes in multiple drug-resistant plasmids of S. Typhimurium strains from hospitals of different countries. Z. Gesamte Hyg. 33, (1987) 264–266 (German).Google Scholar
  55. 55.
    Rabsch, W., Tschäpe, H., Tietze, E., and Kuhn, H. (1982) Characterization of individual Salmonella clones of an epidemic strain of the same phageand biochemotype using plasmid determination. Z. Gesamte Hyg. 28, 842–844 (German).PubMedGoogle Scholar
  56. 56.
    Böhme, G., Kühn., H., Tschape, H., and Rabsch, W. (1989) Epidemiology of salmonellosis. Z. Gesamte Hyg. 35, 638–640 (German).PubMedGoogle Scholar
  57. 57.
    Jacob, W. K., Kuhn, H., Kurschner, H., and Rabsch, W. (1993) The epidemiological analysis of Salmonella Typhimurium infections in cattle — results of lysotyping and biochemotyping in the region of East Thuringia from 1974 to 1991. Berl. Munch. Tierarztl. Wochenschr. 106, 265–269 (German).PubMedGoogle Scholar
  58. 58.
    Kühn, H., Rabsch, W., and Liesegang, A. (1994) Current epidemiological status of salmonellosis of humans in Germany (Review). Immun. Infekt. 22, 4–9 (German).PubMedGoogle Scholar
  59. 59.
    Aiogaily, Z., Anastassiadou, H., Barrow, P. A., et al. (1994) Control of Salmonella infections in animals and prevention of human foodborne Salmonella infections. Bull. World Health Organ. 72, 831–833.Google Scholar
  60. 60.
    Ang-Kücüker, M., Tolun, V., Helmuth, R., et al. (2000) Phage types antibiotic susceptibilities and plasmid profiles of Salmonella Typhimurium and Salmonella Enteritidis strains isolated in Istanbul, Turkey. Clin. Microbiol. Infect. 6, 593–599.CrossRefPubMedGoogle Scholar
  61. 61.
    Rabsch, W., Tschäpe, H., and Bäumler, A. J. (2001) Non-typhoidal Salmonellosis: emerging problems. Microbes Infect. 3, 237–247.CrossRefPubMedGoogle Scholar
  62. 62.
    Helms, M., Ethelberg, S., and Molbak, K. (2005) DT104 Study Group. International Salmonella Typhimurium DT104 infections, 1992–2001. Emerg. Infect. Dis. (Jun) 11, 859–867.PubMedGoogle Scholar
  63. 63.
    Rabsch, W., Andrews, H. L., Kingsley, R. A., Prager, R., and Tschäpe, H. (2002) Salmonella enterica serotype Typhimurium and its host-adapted Variants. Infect. Immun. 70, 2249–2255.CrossRefPubMedGoogle Scholar
  64. 64.
    Frech, G., Weide-Botjes, M., Nußbeck, E., Rabsch, W., and Schwarz, S. (1998) Molecular characterization of Salmonella enterica subspec. enterica serovar Typhimurium DT 009 isolates: differentiation of the live vaccine strain Zoosaloral H from field isolates. FEMS Microbiol. Lett. 167, 263–269.CrossRefPubMedGoogle Scholar
  65. 65.
    Rabsch, W., Liesegang, A., and Tschäpe, H. (2001) Laboratory-based surveillance of salmonellosis of humans in Germany — safety of Salmonella Typhimurium and Salmonella Enteritidis live vaccines. Berl. Munch. Tierarztl. Wochenschr. 114, 433–437 (German) Reprints English from the author.PubMedGoogle Scholar
  66. 66.
    Hashemolhosseini, S., Holmes, Z., Mutschler, B., and Henning, U. (1994) Alterations of receptor specificities of coliphages of the T2 family. J. Mol. Biol. 240, 105–110.CrossRefPubMedGoogle Scholar
  67. 67.
    Luckey, M. and Nikaido, H. (1980) Diffusion of solutes through channels produced by phage lambda receptor protein of Escherichia coli: inhibition by higher oligosaccharides of maltose series. Biochem. Biophys. Res. Commun. 93, 166–171.CrossRefPubMedGoogle Scholar
  68. 68.
    Lucey, M. and Neilands, J. B. (1976) Iron transport in Salmonella Typhimurium LT2: prevention by ferrichrome of adsorption of bacteriophages ES18 and ES18h1 to a common cell envelope receptor. J. Bacteriol. 127, 1036–1037.Google Scholar
  69. 69.
    Schmieger, H. (1999) Molecular survey of the Salmonella phage typing system of Anderson. J. Bacteriol. 181, 1630–1635.PubMedGoogle Scholar
  70. 70.
    Rabsch, W., Mirold, S., Hardt, W. D., and Tschäpe, H. (2002) The dual role of wild phages for horizontal gene transfer among Salmonella strains. Berl. Munch. Tierarztl. Wochenschr. 115, 355–359.PubMedGoogle Scholar
  71. 71.
    Bossi, L. and Bossi, N. F. (2005) Prophage Arsenal of Salmonella enterica Serovar Typhimurium, in Phages — Their Role in Bacterial Pathogenesis and Biotechnology (Waldor, M. K., Friedman, D. I., and Adhya, S. L., eds.), ASM Press Washington, D. C., pp. 165–186.Google Scholar
  72. 72.
    Schloesser, E. (1997) 3. Mikrobiologische Arbeitsmethoden, in Methoden der Bodenbiologie, 2nd edition, (Dunger, W. and Fiedler, H. J., eds.), Gustav Fischer Verlag Jena Stuttgart Lübeck Ulm, p. 92 (German).Google Scholar
  73. 73.
    Rabsch, W. 1995. Klassische epidemiologische Laboratoriumsmethoden, in Salmonellosen des Menschen — Epidemiologische und ätiologische Aspekte. RKI-Schriften 3/95, MMW Medizin Verlag München, pp. 118–134 (German).Google Scholar
  74. 74.
    Rabsch, W., Helm, R. A., and Eisenstark, A. (2004) Diversity of phage types among archived cultures of the Demerec collect of Salmonella enterica serovar Typhimurium strains. Appl. Environ. Microbiol. 70, 664–669.CrossRefPubMedGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2007

Authors and Affiliations

  • Wolfgang Rabsch
    • 1
  1. 1.Robert-Koch Institut, Wernigerode BranchNational Reference Centre for Salmonellae and Other EntericsWernigerodeGermany

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