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PMID: 10531212 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Analysis of virulence of clinical isolates of Salmonella enteritidis in vivo and in vitro.

Infection and immunity ·Vol. 67 ·No. 11 ·1999-11-00 ·Pages 5651-7

Lu S, Manges AR, Xu Y, Fang FC, Riley LW

Abstract

Salmonella enterica serotype Enteritidis (S. enteritidis) is a major food-borne pathogen, and its incidence among all Salmonella serotypes has increased dramatically in the last two decades. To study the virulence characteristics of clinical isolates of S. enteritidis, we determined the 50% lethal doses (LD(50)) in mice of isolates of two major phage types (4 and 8). Isolates of both phage types showed a wide range of LD(50) after oral inoculation, varying from under 10(2) organisms to over 10(8) organisms. No significant difference in LD(50) was observed between the phage types. These observations indicated that clinical isolates of S. enteritidis are highly heterogeneous in their ability to cause death in mice. We compared the LD(50)s of these isolates to the results observed from in vitro pathogenicity assays. We also analyzed these isolates for recognized Salmonella virulence loci (spv, sodCI, sopE, and sef). The in vitro phenotypes of the isolates showed no obvious correlation with their LD(50) in any given assay, and the virulence genes tested were present in all isolates. However, the isolate with the lowest LD(50) (isolate 97A 2472) was resistant to acidified sodium nitrite (ASN). Moreover, the most acid-susceptible, macrophage-susceptible, and ASN-susceptible isolates were attenuated for virulence in mice. These results, based on extensive analysis of clinical isolates of S. enteritidis, demonstrate the complex nature of Salmonella pathogenesis in mice. Our results also indicate the limitation of in vitro assays in predicting in vivo virulence.

MeSH Terms
Animals Female HeLa Cells Humans Lethal Dose 50 Macrophages, Peritoneal/microbiology Mice Mice, Inbred BALB C Nitric Oxide/physiology Plasmids Reactive Oxygen Species Salmonella enteritidis/genetics,pathogenicity Virulence
Chemicals
Reactive Oxygen Species Nitric Oxide
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lu S
Program in Infectious Diseases, School of Public Health, University of California at Berkeley, Berkeley, California, USA.
Manges A R
Xu Y
Fang F C
Riley L W
References (40)
40 references, click to expand
  1. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13997-4001 PMID: 9391141
  2. NO inhibitions: antimicrobial properties of nitric oxide.
    Clin Infect Dis. 1995 Oct;21 Suppl 2:S162-5 PMID: 8845445
  3. Summary of notifiable diseases, United States, 1997.
    MMWR Morb Mortal Wkly Rep. 1998 Nov 20;46(54):ii-vii, 3-87 PMID: 10075376
  4. Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7502-7 PMID: 10377444
  5. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium.
    Am J Pathol. 1967 Jan;50(1):109-36 PMID: 5334433
  6. A multiple plasmid-containing Escherichia coli strain: convenient source of size reference plasmid molecules.
    Plasmid. 1978 Jun;1(3):417-20 PMID: 372973
  7. Inversions between ribosomal RNA genes of Escherichia coli.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):7069-72 PMID: 6273909
  8. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189-93 PMID: 3523484
  9. Characterization of plasmids conferring resistance to gentamicin and apramycin in strains of Salmonella typhimurium phage type 204c isolated in Britain.
    J Hyg (Lond). 1986 Dec;97(3):419-26 PMID: 3540111
  10. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study.
    Microbiol Immunol. 1986;30(12):1225-37 PMID: 3553868
  11. A phage-typing scheme for Salmonella enteritidis.
    Epidemiol Infect. 1987 Oct;99(2):291-4 PMID: 3315705
  12. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages.
    Infect Immun. 1989 Jan;57(1):1-7 PMID: 2642463
  13. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells.
    J Exp Med. 1989 May 1;169(5):1543-55 PMID: 2497225
  14. Studies on early association of Salmonella typhimurium with intestinal mucosa in vivo and in vitro: relationship to virulence.
    J Med Microbiol. 1989 Aug;29(4):283-94 PMID: 2668530
  15. Correlation between the presence of sequences homologous to the vir region of Salmonella dublin plasmid pSDL2 and the virulence of twenty-two Salmonella serotypes in mice.
    Infect Immun. 1990 May;58(5):1180-5 PMID: 2323813
  16. Peroxidase-antiperoxidase and immunogold labeling of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf in tissues of experimentally infected swine.
    Am J Vet Res. 1990 Apr;51(4):619-24 PMID: 2183652
  17. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium.
    Infect Immun. 1990 Jun;58(6):2014-6 PMID: 1971262
  18. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4304-8 PMID: 2349239
  19. Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle 407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein.
    Infect Immun. 1991 Jan;59(1):437-40 PMID: 1987056
  20. Role of nitric oxide synthesis in macrophage antimicrobial activity.
    Curr Opin Immunol. 1991 Feb;3(1):65-70 PMID: 1711326
  21. Growth regulation of a Salmonella plasmid gene essential for virulence.
    J Bacteriol. 1991 Nov;173(21):6783-9 PMID: 1938884
  22. Intracellular replication is essential for the virulence of Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11470-4 PMID: 1763061
  23. Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1847-51 PMID: 1311853
  24. The alternative sigma factor katF (rpoS) regulates Salmonella virulence.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11978-82 PMID: 1465428
  25. The changing epidemiology of foodborne diseases.
    Am J Med Sci. 1996 Jan;311(1):23-9 PMID: 8571982
  26. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium.
    Science. 1996 Apr 19;272(5260):414-7 PMID: 8602531
  27. Salmonellosis: host immune responses and bacterial virulence determinants.
    Annu Rev Immunol. 1996;14:533-61 PMID: 8717524
  28. Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defense.
    Antimicrob Agents Chemother. 1996 Jun;40(6):1422-5 PMID: 8726013
  29. Recurrent outbreaks of Salmonella Enteritidis infections in a Texas restaurant: phage type 4 arrives in the United States.
    Epidemiol Infect. 1996 Aug;117(1):29-34 PMID: 8760947
  30. Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens.
    Epidemiol Infect. 1996 Aug;117(1):79-88 PMID: 8760953
  31. Chemical synthesis of nitric oxide in the stomach from dietary nitrate in humans.
    Gut. 1997 Feb;40(2):211-4 PMID: 9071933
  32. A novel antioxidant gene from Mycobacterium tuberculosis.
    J Exp Med. 1997 Dec 1;186(11):1885-96 PMID: 9382887
  33. A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks.
    Epidemiol Infect. 1993 Feb;110(1):17-22 PMID: 8432319
  34. Cloning, DNA nucleotide sequence and distribution of the gene encoding the SEF14 fimbrial antigen of Salmonella enteritidis.
    J Gen Microbiol. 1993 Jul;139(7):1477-85 PMID: 8371111
  35. Outbreaks of Salmonella enteritidis infections in the United States, 1985-1991.
    J Infect Dis. 1994 Mar;169(3):547-52 PMID: 8158026
  36. Determination of median lethal and infectious doses in animal model systems.
    Methods Enzymol. 1994;235:29-39 PMID: 8057901
  37. Invasion and intracellular proliferation of Salmonella within non-phagocytic cells.
    Microbiologia. 1994 Sep;10(3):229-38 PMID: 7873099
  38. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6399-403 PMID: 7604003
  39. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate.
    Nat Med. 1995 Jun;1(6):546-51 PMID: 7585121
  40. A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2574-9 PMID: 9482928
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
DOI
10.1128/IAI.67.11.5651-5657.1999
Published
1999-11-00
Pages
5651-7
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC96938
Subset
IM
Grants
NIAID NIH HHS · R01 AI039557 · United States
NIAID NIH HHS · AI39557 · United States
NIAID NIH HHS · AI43032 · United States
External Links
PubMed source DOI: 10.1128/IAI.67.11.5651-5657.1999 PMC Full Text View journal details
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