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Home / Equine Research Bank / Appl Environ Microbiol / Enterotoxigenic potential of Staphylococcus intermedius.
Applied and environmental microbiology2001; 67(12); 5551-5557; doi: 10.1128/AEM.67.12.5551-5557.2001

Enterotoxigenic potential of Staphylococcus intermedius.

Abstract: Staphylococcal food poisoning (SFP) caused by enterotoxigenic staphylococci is one of the main food-borne diseases. In contrast to Staphylococcus aureus, a systematic screening for the enterotoxins has not yet been performed on the genomic level for the coagulase-positive species S. intermedius. Therefore, the enterotoxigenic potential of 281 different veterinary (canine, n = 247; equine, n = 23; feline, n = 9; other, n = 2) and 11 human isolates of S. intermedius was tested by using a multiplex PCR DNA-enzyme immunoassay system targeting the staphylococcal enterotoxin genes sea, seb, sec, sed, and see. Molecular results were compared by in vitro testing of enterotoxin production by two immunoassays. A total of 33 (11.3%) S. intermedius isolates, including 31 (12.6%) canine isolates, 1 equine isolate, and 1 human isolate, tested positive for the sec gene. In vitro production of the respective enterotoxins was detected in 30 (90.9%) of these isolates by using immunological tests. In contrast, none of 65 veterinary specimen-derived isolates additionally tested and comprising 13 (sub)species of coagulase-negative staphylococci were found to be enterotoxigenic. This study shows on both molecular and immunological levels that a substantial number of S. intermedius isolates harbor the potential for enterotoxin production. Since evidence for noninvasive zoonotic transmission of S. intermedius from animal hosts to humans has been documented, an enterotoxigenic role of this microorganism in SFP via contamination of food products may be assumed.
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Publication Date: 2001-11-28 PubMed ID: 11722906PubMed Central: PMC93343DOI: 10.1128/AEM.67.12.5551-5557.2001Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study explores the potential of Staphylococcus intermedius, a bacterium often found in animals, to produce enterotoxins that can cause food poisoning in humans. Through molecular and immunological testing of 281 veterinary and 11 human isolates, it was found that a significant number of these samples had the potential to produce harmful enterotoxins.

Study Overview

  • The research involved testing the enterotoxigenic potential of 281 veterinary (mainly from dogs but also horses, cats, and others) and 11 human isolates of Staphylococcus intermedius. This bacterium is commonly associated with animals, particularly dogs, but it is also known to occasionally cause infections in humans.
  • The testing was done using a multiplex PCR DNA-enzyme immunoassay that targeted specific enterotoxin genes — sea, seb, sec, sed, and see. These genes are associated with the production of enterotoxins, which are toxins that cause food poisoning when ingested.
  • In addition to the molecular testing, the team also conducted in vitro testing of enterotoxin production using two immunoassays. This was done to compare the results with the molecular tests.

Key Findings

  • Of the Staphylococcus intermedius isolates tested, 33 (11.3%) were found to contain the sec gene, an enterotoxin gene. The detection of an enterotoxin gene in these isolates suggests they have the potential to produce toxins that cause food poisoning.
  • The sec gene was found in a larger proportion of canine isolates (12.6%) compared to other species. It was also found in one equine isolate and one human isolate.
  • Immunological tests confirmed the production of enterotoxins in 90.9% of the positive isolates, thus validating the molecular results.
  • None of the additional 65 veterinary isolates from different species of coagulase-negative staphylococci were found to be enterotoxigenic, indicating that the enterotoxin-producing potential may be specific to S. intermedius among the tested bacteria.

Implications and Conclusions

  • The findings of this study show that S. intermedius has a substantial potential to produce enterotoxins that can cause food poisoning in humans.
  • Given the documented cases of S. intermedius transmission from animal to humans, it is suggested that food contamination by this bacterium could potentially lead to staphylococcal food poisoning.
  • Despite the prevalence of S. intermedius being largely associated with animals, its potential as a human pathogen due to its enterotoxigenic properties is significant and warrants further investigation.

Cite This Article

APA
Becker K, Keller B, von Eiff C, Brück M, Lubritz G, Etienne J, Peters G. (2001). Enterotoxigenic potential of Staphylococcus intermedius. Appl Environ Microbiol, 67(12), 5551-5557. https://doi.org/10.1128/AEM.67.12.5551-5557.2001

Publication

Applied and environmental microbiology
ISSN: 0099-2240
NlmUniqueID: 7605801
Country: United States
Language: English
Volume: 67
Issue: 12
Pages: 5551-5557

Researcher Affiliations

Becker, K
  • Institute of Medical Microbiology, University of Münster, 48149 Münster, Germany. kbecker@uni-muenster.de
Keller, B
    von Eiff, C
      Brück, M
        Lubritz, G
          Etienne, J
            Peters, G

              MeSH Terms

              • Animals
              • Base Sequence
              • Cat Diseases / microbiology
              • Cats
              • Dog Diseases / microbiology
              • Dogs
              • Enterotoxins / genetics
              • Enterotoxins / metabolism
              • Guinea Pigs
              • Horse Diseases / microbiology
              • Horses
              • Humans
              • Immunoenzyme Techniques
              • Molecular Sequence Data
              • Polymerase Chain Reaction
              • Rabbits
              • Staphylococcal Infections / microbiology
              • Staphylococcal Infections / veterinary
              • Staphylococcus / classification
              • Staphylococcus / genetics
              • Staphylococcus / isolation & purification
              • Staphylococcus / metabolism

              References

              This article includes 66 references
              1. al Bustan M A, Udo E E, Chugh T D. Nasal carriage of enterotoxin-producing Staphylococcus aureus among restaurant workers in Kuwait City.. Epidemiol Infect 1996;116:319–322.
                pmc: PMC2271425pubmed: 8666076
              2. Allaker R P, Lloyd D H, Bailey R M. Population sizes and frequency of staphylococci at mucocutaneous sites on healthy dogs.. Vet Rec 1992;130:303–304.
                pubmed: 1595151
              3. Allaker R P, Lloyd D H, Simpson A I. Occurrence of Staphylococcus intermedius on the hair and skin of normal dogs.. Res Vet Sci 1992;52:174–176.
                pubmed: 1585075
              4. Almazan J, de la Fuente R, Gomez Lucía E, Suárez G. Enterotoxin production by strains of Staphylococcus intermedius and Staphylococcus aureus isolated from dog infections.. Zentbl Bakteriol Mikrobiol Hyg A 1987;264:29–32.
                pubmed: 3630476
              5. Altekruse S F, Cohen M L, Swerdlow D L. Emerging foodborne diseases.. Emerg Infect Dis 1997;3:285–293.
                pmc: PMC2627632pubmed: 9284372
              6. Archer D L, Young F E. Contemporary issues: diseases with a food vector.. Clin Microbiol Rev 1988;1:377–398.
                pmc: PMC358061pubmed: 3069199
              7. Balaban N, Rasooly A. Staphylococcal enterotoxins.. Int J Food Microbiol 2000;61:1–10.
                pubmed: 11028954
              8. Barg N L, Harris T. Toxin-mediated syndromes.. The staphylococci in human disease 1997. pp. 527–543.
              9. Becker K, Roth R, Peters G. Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene.. J Clin Microbiol 1998;36:2548–2553.
                pmc: PMC105160pubmed: 9705390
              10. Bennett R W. Atypical toxigenic Staphylococcus and non-Staphylococcus aureus species on the horizon? An update.. J Food Prot 1996;59:1123–1126.
                pubmed: 31195457
              11. Berg J N, Wendell D E, Vogelweid C, Fales W H. Identification of the major coagulase-positive Staphylococcus sp. of dogs as Staphylococcus intermedius.. Am J Vet Res 1984;45:1307–1309.
                pubmed: 24049888
              12. Bergdoll M S. Enterotoxins.. Staphylococci and staphylococcal infections 1983. pp. 559–598.
              13. Bergdoll M S. Importance of staphylococci that produce nanogram quantities of enterotoxin.. Zentbl Bakteriol 1995;282:1–6.
                pubmed: 7734822
              14. Berry P R, Wieneke A A, Rodhouse J C, Gilbert R J. Use of commercial kits for the detection of Clostridium perfringens and Staphylococcus aureus enterotoxins.. Immunological techniques in microbiology 1987. pp. 245–254.
              15. Betley M J, Borst D W, Regassa L B. Staphylococcal enterotoxins, toxic shock syndrome toxin and streptococcal pyrogenic exotoxins: a comparative study of their molecular biology.. Chem Immunol 1992;55:1–35.
                pubmed: 1418613
              16. Biberstein E L, Jang S S, Hirsh D C. Species distribution of coagulase-positive staphylococci in animals.. J Clin Microbiol 1984;19:610–615.
                pmc: PMC271141pubmed: 6429188
              17. Bohach G A. Staphylococcal enterotoxins B and C. Structural requirements for superantigenic and enterotoxigenic activities.. Prep Biochem Biotechnol 1997;27:79–110.
                pubmed: 9292922
              18. Bohach G A, Fast D J, Nelson R D, Schlievert P M. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses.. Crit Rev Microbiol 1990;17:251–272.
                pubmed: 2206394
              19. Bohach G A, Foster T J. Staphylococcus aureus exotoxins.. Gram-positive pathogens 2000. pp. 367–378.
              20. Bohach G A, Schlievert P M. Nucleotide sequence of the staphylococcal enterotoxin C1 gene and relatedness to other pyrogenic toxins.. Mol Gen Genet 1987;209:15–20.
                pubmed: 2823067
              21. Bohach G A, Schlievert P M. Conservation of the biologically active portions of staphylococcal enterotoxins C1 and C2.. Infect Immun 1989;57:2249–2252.
                pmc: PMC313868pubmed: 2543637
              22. Brakstad O G, Aasbakk K, Maeland J A. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene.. J Clin Microbiol 1992;30:1654–1660.
                pmc: PMC265359pubmed: 1629319
              23. Breckinridge J C, Bergdoll M S. Outbreak of food-borne gastroenteritis due to a coagulase-negative staphylococcus.. N Engl J Med 1971;284:541–543.
                pubmed: 5542573
              24. Burkett G, Frank L A. Comparison of production of Staphylococcus intermedius exotoxin among clinically normal dogs, atopic dogs with recurrent pyoderma, and dogs with a single episode of pyoderma.. J Am Vet Med Assoc 1998;213:232–234.
                pubmed: 9676593
              25. Chou C C, Chen L F. Enterotoxin production by Staphylococcus warneri CCRC 12929, a coagulase-negative strain.. J Food Prot 1997;60:923–927.
                pubmed: 31207796
              26. Couch J L, Betley M J. Nucleotide sequence of the type C3 staphylococcal enterotoxin gene suggests that intergenic recombination causes antigenic variation.. J Bacteriol 1989;171:4507–4510.
                pmc: PMC210234pubmed: 2473979
              27. Cox H U, Hoskins J D, Newman S S, Foil C S, Turnwald G H, Roy A F. Temporal study of staphylococcal species on healthy dogs.. Am J Vet Res 1988;49:747–751.
                pubmed: 3400910
              28. Crowle A J. Immunodiffusion.. 1961.
              29. Devriese L A, Nzuambe D, Godard C. Identification and characteristics of staphylococci isolated from lesions and normal skin of horses.. Vet Microbiol 1985;10:269–277.
                pubmed: 3159146
              30. Dinges M M, Orwin P M, Schlievert P M. Exotoxins of Staphylococcus aureus.. Clin Microbiol Rev 2000;13:16–34.
                pmc: PMC88931pubmed: 10627489
              31. Dziewanowska K, Edwards V M, Deringer J R, Bohach G A, Guerra D J. Comparison of the beta-toxins from Staphylococcus aureus and Staphylococcus intermedius.. Arch Biochem Biophys 1996;335:102–108.
                pubmed: 8914839
              32. Edwards V M, Deringer J R, Callantine S D, Deobald C F, Berger P H, Kapur V, Staﾬher C V, Bohach G A. Characterization of the canine type C enterotoxin produced by Staphylococcus intermedius pyoderma isolates.. Infect Immun 1997;65:2346–2352.
                pmc: PMC175325pubmed: 9169773
              33. Goh S H, Byrne S K, Zhang J L, Chow A W. Molecular typing of Staphylococcus aureus on the basis of coagulase gene polymorphisms.. J Clin Microbiol 1992;30:1642–1645.
                pmc: PMC265357pubmed: 1352784
              34. Gomez Lucía E, Goyache J, Orden J A, Blanco J L, Ruiz Santa Quiteria J A, Domínguez L, Suárez G. Production of enterotoxin A by supposedly nonenterotoxigenic Staphylococcus aureus strains.. Appl Environ Microbiol 1989;55:1447–1451.
                pmc: PMC202884pubmed: 2764561
              35. Greene R T, Lämmler C. Staphylococcus intermedius: current knowledge on a pathogen of veterinary importance.. Zentbl Veterinärmed B 1993;40:206–214.
                pubmed: 8342369
              36. Hajek V. Staphylococcus intermedius, a new species isolated from animals.. Int J Syst Bacteriol 1976;26:401–408.
              37. Hirooka E Y, Muller E E, Freitas J C, Vicente E, Yoshimoto Y, Bergdoll M S. Enterotoxigenicity of Staphylococcus intermedius of canine origin.. Int J Food Microbiol 1988;7:185–191.
                pubmed: 3275321
              38. Inganäs M, Johansson S G, Bennich H H. Interaction of human polyclonal IgE and IgG from different species with protein A from Staphylococcus aureus: demonstration of protein-A-reactive sites located in the Fab2 fragment of human IgG.. Scand J Immunol 1980;12:23–31.
                pubmed: 6158089
              39. Jarraud S, Peyrat M A, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus.. J Immunol 2001;166:669–677.
                pubmed: 11123352
              40. Jay J M. Modern food microbiology.. 1996. pp. 429–450.
              41. Khambaty F M, Bennett R W, Shah D B. Application of pulsed-field gel electrophoresis to the epidemiological characterization of Staphylococcus intermedius implicated in a food-related outbreak.. Epidemiol Infect 1994;113:75–81.
                pmc: PMC2271228pubmed: 8062882
              42. Kotb M. Bacterial pyrogenic exotoxins as superantigens.. Clin Microbiol Rev 1995;8:411–426.
                pmc: PMC174633pubmed: 7553574
              43. Lee J. Staphylococcus intermedius isolated from dog-bite wounds.. J Infect 1994;29:105.
                pubmed: 7963622
              44. Lehn N, Schaller E, Wagner H, Krönke M. Frequency of toxic shock syndrome toxin- and enterotoxin-producing clinical isolates of Staphylococcus aureus.. Eur J Clin Microbiol Infect Dis 1995;14:43–46.
                pubmed: 7729452
              45. Llorca I, Gago S, Sanmartin J, Sanchez R. Endocarditis infecciosa por Staphylococcus intermedius en paciente infectado por VIH.. Enferm Infecc Microbiol Clin 1992;10:317–318.
                pubmed: 1391010
              46. Marin M E, de la Rosa M C, Cornejo I. Enterotoxigenicity of Staphylococcus strains isolated from Spanish dry-cured hams.. Appl Environ Microbiol 1992;58:1067–1069.
                pmc: PMC195384pubmed: 1575480
              47. Marrack P, Kappler J. The staphylococcal enterotoxins and their relatives.. Science 1990;248:705–711.
                pubmed: 2185544
              48. Medleau L, Blue J L. Frequency and antimicrobial susceptibility of Staphylococcus spp isolated from feline skin lesions.. J Am Vet Med Assoc 1988;193:1080–1081.
                pubmed: 3198459
              49. Mendoza M, Meugnier H, Bes M, Etienne J, Freney J. Identification of Staphylococcus species by 16S–23S rDNA intergenic spacer PCR analysis.. Int J Syst Bacteriol 1998;48:1049–1055.
                pubmed: 9734063
              50. Miyake Y, Iwai T, Sugai M, Miura K, Suginaka H, Nagasaka N. Incidence and characterization of Staphylococcus aureus from the tongues of children.. J Dent Res 1991;70:1045–1047.
                pubmed: 2066485
              51. Munson S H, Tremaine M T, Betley M J, Welch R A. Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus.. Infect Immun 1998;66:3337–3348.
                pmc: PMC108350pubmed: 9632603
              52. Orden J A, Cid D, Blanco M E, Ruiz Santa Quiteria J A, Gomez Lucía E, de la Fuente R. Enterotoxin and toxic shock syndrome toxin-one production by staphylococci isolated from mastitis in sheep.. APMIS 1992;100:132–134.
                pubmed: 1554486
              53. Park C E, Akhtar M, Rayman M K. Nonspecific reactions of a commercial enzyme-linked immunosorbent assay kit (TECRA) for detection of staphylococcal enterotoxins in foods.. Appl Environ Microbiol 1992;58:2509–2512.
                pmc: PMC195813pubmed: 1514798
              54. Raus J, Love D N. Characterization of coagulase-positive Staphylococcus intermedius and Staphylococcus aureus isolated from veterinary clinical specimens.. J Clin Microbiol 1983;18:789–792.
                pmc: PMC270907pubmed: 6630462
              55. Ren K, Bannan J D, Pancholi V, Cheung A L, Robbins J C, Fischetti V A, Zabriskie J B. Characterization and biological properties of a new staphylococcal exotoxin.. J Exp Med 1994;180:1675–1683.
                pmc: PMC2191734pubmed: 7964453
              56. Rifai S, Barbancon V, Prevost G, Piemont Y. Synthetic exfoliative toxin A and B DNA probes for detection of toxigenic Staphylococcus aureus strains.. J Clin Microbiol 1989;27:504–506.
                pmc: PMC267347pubmed: 2715322
              57. Rosec J P, Guiraud J P, Dalet C, Richard N. Enterotoxin production by staphylococci isolated from foods in France.. Int J Food Microbiol 1997;35:213–221.
                pubmed: 9105930
              58. Surgalla M J, Bergdoll M S, Dack G M. Some observations on the assay of staphylococcal enterotoxin by the monkey-feeding test.. J Lab Clin Med 1953;41:782–788.
                pubmed: 13053035
              59. Talan D A, Staatz D, Staatz A, Goldstein E J, Singer K, Overturf G D. Staphylococcus intermedius in canine gingiva and canine-inflicted human wound infections: laboratory characterization of a newly recognized zoonotic pathogen.. J Clin Microbiol 1989;27:78–81.
                pmc: PMC267236pubmed: 2913039
              60. Talan D A, Staatz D, Staatz A, Overturf G D. Frequency of Staphylococcus intermedius as human nasopharyngeal flora.. J Clin Microbiol 1989;27:2393.
                pmc: PMC267035pubmed: 2584388
              61. Tanner M A, Everett C L, Youvan D C. Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human.. J Clin Microbiol 2000;38:1628–1631.
                pmc: PMC86505pubmed: 10747154
              62. Todd E C. Costs of acute bacterial foodborne disease in Canada and the United States.. Int J Food Microbiol 1989;9:313–326.
                pubmed: 2701860
              63. Valle J, Gomez-Lucia E, Piriz S, Goyache J, Orden J A, Vadillo S. Enterotoxin production by staphylococci isolated from healthy goats.. Appl Environ Microbiol 1990;56:1323–1326.
                pmc: PMC184403pubmed: 2339886
              64. Vandenesch F, Célard M, Arpin D, Bes M, Greenland T, Etienne J. Catheter-related bacteremia associated with coagulase-positive Staphylococcus intermedius.. J Clin Microbiol 1995;33:2508–2510.
                pmc: PMC228460pubmed: 7494062
              65. Vernozy Rozand C, Mazuy C, Prevost G, Lapeyre C, Bes M, Brun Y, Fleurette J. Enterotoxin production by coagulase-negative staphylococci isolated from goats' milk and cheese.. Int J Food Microbiol 1996;30:271–280.
                pubmed: 8854180
              66. Zhang S, Iandolo J J, Stewart G C. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol Lett 1998;168:227–233.
                pubmed: 9835033
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