1887

Abstract

serovar Enteritidis is unable to multiply in the albumen of fresh eggs and must gain access to the yolk contents in order to multiply to a high level (>10 c.f.u. per ml egg contents). As human infections resulting from the consumption of infected eggs more frequently involve serovar Enteritidis phage type (PT) 4 than other serovars or PTs, a number of isolates of various serovars were examined for their ability to multiply to a high level in eggs over a period of 8 days storage at 20 °C. Their behaviour was compared to that of a range of defined fimbrial and flagella mutants of . Enteritidis. Strains that did not express flagella were unable to multiply in eggs, and those deficient for curli fimbriae, including strains of . Enteritidis PT6, displayed high-level growth in significantly fewer eggs than those able to express curli. Most . Enteritidis strains multiplied to a high level in between 5 and 10 % of eggs during 8 days storage. One PT4 strain, though, showed high levels of growth in more than 25 % of eggs over this period, significantly higher than the other PTs or the two other isolates of PT4 tested. This ability may be important for the association of PT4 infection with the consumption of eggs.

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2004-04-01
2019-10-21
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References

  1. Allen-Vercoe, E. & Woodward, M. J. ( 1999; ). The role of flagella, but not fimbriae, in the adherence of Salmonella enterica serotype Enteritidis to chick gut explant. J Med Microbiol 48, 771–780.[CrossRef]
    [Google Scholar]
  2. Allen-Vercoe, E., Collighan, R. & Woodward, M. J. ( 1998; ). The variant rpoS allele of S. enteritidis strain 27655R does not affect virulence in a chick model nor constitutive curliation but does generate a cold-sensitive phenotype. FEMS Microbiol Lett 167, 245–253.[CrossRef]
    [Google Scholar]
  3. Allen-Vercoe, E., Sayers, A. R. & Woodward, M. J. ( 1999; ). Virulence of Salmonella enterica serotype Enteritidis aflagellate and afimbriate mutants in a day-old chick model. Epidemiol Infect 122, 395–402.[CrossRef]
    [Google Scholar]
  4. Baron, F., Gautier, M. & Brule, G. ( 1997; ). Factors involved in the inhibition of growth of Salmonella enteritidis in liquid egg white. J Food Prot 60, 1318–1323.
    [Google Scholar]
  5. Bellairs, R., Harkness, M. & Harkness, R. D. ( 1963; ). The vitelline membrane of the hen's egg: a chemical and electron microscopical study. J Ultrastruct Res 8, 339–359.[CrossRef]
    [Google Scholar]
  6. Board, R. G. ( 1964; ). The growth of Gram-negative bacteria in the hen's egg. J Appl Bacteriol 27, 350–364.[CrossRef]
    [Google Scholar]
  7. Clay, C. E. & Board, R. G. ( 1991; ). Growth of Salmonella enteritidis in artificially contaminated hens' shell eggs. Epidemiol Infect 106, 271–281.[CrossRef]
    [Google Scholar]
  8. Cogan, T. A., Domingue, G., Lappin-Scott, H., Benson, C. E., Woodward, M. J. & Humphrey, T. J. ( 2001; ). Growth of Salmonella enterica Serovar Enteritidis in artificially contaminated eggs: the influence of inoculum size and suspending media. Int J Food Microbiol 70, 131–141.[CrossRef]
    [Google Scholar]
  9. Collinson, S. K., Emody, L., Muller, K. H., Trust, T. J. & Kay, W. W. ( 1991; ). Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol 173, 4773–4781.
    [Google Scholar]
  10. Dibb-Fuller, M. P., Allen-Vercoe, E., Thorns, C. J. & Woodward, M. J. ( 1999; ). Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145, 1023–1031.[CrossRef]
    [Google Scholar]
  11. Garcia, F. J., Pons, A., Alemany, M. & Palou, A. ( 1983; ). Permeability of chicken egg vitelline membrane to glucose, carbohydrate gradients between albumen and yolk. Comp Biochem Physiol B 75, 137–140.
    [Google Scholar]
  12. Gast, R. K. & Holt, P. S. ( 2000; ). Deposition of phage type 4 and 13a Salmonella enteritidis strains in the yolk and albumen of eggs laid by experimentally infected hens. Avian Dis 44, 706–710.[CrossRef]
    [Google Scholar]
  13. Gerstel, U. & Römling, U. ( 2001; ). Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3, 638–648.[CrossRef]
    [Google Scholar]
  14. Holt, P. S. & Chaubal, L. H. ( 1997; ). Detection of motility and putative synthesis of flagellar proteins in Salmonella pullorum cultures. J Clin Microbiol 35, 1016–1020.
    [Google Scholar]
  15. Hosieth, S. K. & Stocker, B. A. D. ( 1981; ). Aromatic-dependent Salmonella typhimurium are not virulent and effective as live vaccines. Nature 291, 238–239.[CrossRef]
    [Google Scholar]
  16. Hotani, H. ( 1971; ). Interconversion between flagella and P-filament in vitro. J Mol Biol 57, 575–587.[CrossRef]
    [Google Scholar]
  17. Humphrey, T. J. ( 1990; ). Growth of salmonellas in intact shell eggs: influence of storage temperature. Vet Rec 126, 292.
    [Google Scholar]
  18. Humphrey, T. J., Baskerville, A., Mawer, S., Rowe, B. & Hopper, S. ( 1989; ). Salmonella enteritidis phage type 4 from the contents of intact eggs: a study involving naturally infected hens. Epidemiol Infect 103, 415–423.[CrossRef]
    [Google Scholar]
  19. Humphrey, T. J., Whitehead, A., Gawler, A. H. L., Henley, A. & Rowe, B. ( 1991; ). Numbers of Salmonella enteritidis in the contents of naturally contaminated hens' eggs. Epidemiol Infect 106, 489–496.[CrossRef]
    [Google Scholar]
  20. Humphrey, T. J., Slater, E., McAlpine, K., Rowbury, R. J. & Gilbert, R. J. ( 1995; ). Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid or hydrogen peroxide also survive longer on surfaces. Appl Environ Microbiol 61, 3161–3164.
    [Google Scholar]
  21. Humphrey, T. J., Wilde, S. J. & Rowbury, R. J. ( 1997; ). Heat tolerance of Salmonella typhimurium DT104 isolates attached to muscle tissue. Lett Appl Microbiol 25, 265–268.[CrossRef]
    [Google Scholar]
  22. Jørgensen, F., Leach, S., Wilde, S. J., Davies, A., Stewart, G. S. & Humphrey, T. ( 2000; ). Invasiveness in chickens, stress resistance and RpoS status of wild-type Salmonella enterica subsp. enterica serovar typhimurium definitive type 104 and serovar enteritidis phage type 4 strains. Microbiology 146, 3227–3235.
    [Google Scholar]
  23. Keller, L. H., Schifferli, D. M., Benson, C. E., Aslam, S. & Eckroade, R. J. ( 1997; ). Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis. Avian Dis 41, 535–539.[CrossRef]
    [Google Scholar]
  24. La Ragione, R. M., Collighan, R. J. & Woodward, M. J. ( 1999; ). Non-curliation of Escherichia coli O78 : K80 isolates associated with IS1 insertion in csgB and reduced persistence in poultry infection. FEMS Microbiol Lett 175, 247–253.[CrossRef]
    [Google Scholar]
  25. La Ragione, R. M., Cooley, W. A. & Woodward, M. J. ( 2000; ). The role of fimbriae and flagella in the adherence of avian strains of Escherichia coli O78 : K80 to tissue culture cells and tracheal and gut explants. J Med Microbiol 49, 327–338.
    [Google Scholar]
  26. Mawer, S. L., Spain, S. E. & Rowe, B. ( 1989; ). Salmonella enteritidis phage type 4 and hens' eggs. Lancet I, 281.
    [Google Scholar]
  27. Moreno, M., Audia, J. P., Bearson, S. M., Webb, C. & Foster, J. W. ( 2000; ). Regulation of sigma S degradation in Salmonella enterica var typhimurium: in vivo interactions between sigma S, the response regulator MviA(RssB) and ClpX. J Mol Microbiol Biotechnol 2, 245–254.
    [Google Scholar]
  28. Ogunniyi, A. D., Kotlarski, I., Morona, R. & Manning, P. A. ( 1997; ). Role of SefA subunit protein of SEF14 fimbriae in the pathogenesis of Salmonella enterica serovar Enteritidis. Infect Immun 65, 708–717.
    [Google Scholar]
  29. Okamura, M., Kamijima, Y., Miyamoto, T., Tani, H., Sasai, K. & Baba, E. ( 2001a; ). Differences among six Salmonella serovars in abilities to colonise reproductive organs and to contaminate eggs in laying hens. Avian Dis 45, 61–69.[CrossRef]
    [Google Scholar]
  30. Okamura, M., Miyamoto, T., Kamijima, Y., Tani, H., Sasai, K. & Baba, E. ( 2001b; ). Differences in abilities to colonise reproductive organs and to contaminate eggs in intravaginally contaminated hens and in vitro adherences to vaginal explants between Salmonella enteritidis and other Salmonella serovars. Avian Dis 45, 962–971.[CrossRef]
    [Google Scholar]
  31. Olsen, J. E., Skov, M. N., Threlfall, E. J. & Brown, D. J. ( 1994; ). Clonal lines of Salmonella enterica serotype Enteritidis documented by IS200, ribo, pulsed field gel electrophoresis and RFLP typing. J Med Microbiol 40, 15–22.[CrossRef]
    [Google Scholar]
  32. Poppe, C. ( 1999; ). Epidemiology of Salmonella enterica serovar Enteritidis. In Salmonella Enterica Serovar Enteritidis in Humans and Animals. Epidemiology, Pathogenesis and Control, pp. 3–18. Edited by A. Saeed. Ames, IA: Iowa State University Press.
  33. Rabsch, W., Tschape, H. & Baumler, A. J. ( 2001; ). Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3, 237–247.[CrossRef]
    [Google Scholar]
  34. Rajashekara, G., Munir, S., Alexeyev, M. F., Halvorson, D. A., Wells, C. L. & Nagaraja, K. V. ( 2000; ). Pathogenic role of SEF14, SEF17 and SEF21 fimbriae in Salmonella enterica serovar enteritidis infection of chickens. Appl Environ Microbiol 66, 1759–1763.[CrossRef]
    [Google Scholar]
  35. Rowbury, R. J. ( 1995; ). An assessment of environmental factors influencing acid tolerance and sensitivity in Escherichia coli, Salmonella spp. and other enterobacteria. Lett Appl Microbiol 20, 333–337.[CrossRef]
    [Google Scholar]
  36. Schade, A. L. & Caroline, L. ( 1944; ). Raw hen egg white and the role of iron in growth inhibition of Shigella dysenteriae, Staphylococcus aureus, Escherichia coli and Saccharomyces cerevisiae. Science 100, 14–15.[CrossRef]
    [Google Scholar]
  37. Shivaprasad, H. L. ( 2000; ). Fowl typhoid and pullorum disease. Rev Sci Tech 19, 405–424.
    [Google Scholar]
  38. Thorns, C. J., Sojka, M. G., McLaren, I. M. & Dibb-Fuller, M. ( 1992; ). Characterisation of monoclonal antibodies against a fimbrial structure of Salmonella enteritidis and certain other serogroup D salmonellae and their application as serotyping reagents. Res Vet Sci 53, 300–308.[CrossRef]
    [Google Scholar]
  39. Turcotte, C. & Woodward, M. J. ( 1993; ). Cloning, DNA nucleotide sequence and distribution of the gene encoding the SEF14 fimbrial antigen of Salmonella enteritidis. J Gen Microbiol 139, 1477–1485.[CrossRef]
    [Google Scholar]
  40. Van Asten, F. J. A. M., Hendriks, H. G. C. J. M., Koninkx, J. F. J. G., Van der Zeijst, B. A. B. & Gaastra, W. ( 2000; ). Inactivation of the flagellin gene of Salmonella enterica serotype Enteritidis strongly reduces invasion into differentiated Caco-2 cells. FEMS Microbiol Lett 185, 175–179.[CrossRef]
    [Google Scholar]
  41. Walker, S. L., Sojka, M. G., Dibb-Fuller, M. & Woodward, M. J. ( 1999; ). Effect of pH, temperature and surface contact on the elaboration of fimbriae and flagella by Salmonella serotype Enteritidis. J Med Microbiol 48, 253–261.[CrossRef]
    [Google Scholar]
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