Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 11/2015

01-11-2015 | Original Article

Prevalence of enterotoxin genes in Staphylococcus aureus colonising food handlers: does nasal carriage status matter?

Authors: J. Ho, M. Boost, M. O’Donoghue

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 11/2015

Login to get access

Abstract

This study investigated the association between the presence of staphylococcal enterotoxin (SE) genes and nasal carriage status, and determined temporal changes in the prevalence of these genes in Staphylococcus aureus strains isolated from healthy carriers between 2002 and 2011. Three large samples of food handlers recruited in 2002, 2003 and 2011 were nasally sampled on two occasions to determine S. aureus colonisation status. Those carrying the same spa type on both occasions were defined as persistent carriers. Genes for SEs SEA–SEU were amplified and associations between carriage status and presence of SE genes were investigated. Although 80 % of nasal isolates harboured at least one SE gene over the sampling period, persistent carriers were significantly more likely to harbour enterotoxigenic S. aureus than transiently colonised subjects [odds ratio (OR) 2.52–3.06]. Strains from persistent carriers more commonly harboured sea, seb and sem. The prevalence of classical SE genes and sej, sem, sen, seo, seq and ses was stable over time, but seh, sel, sep, ser, set and selu increased significantly. Increased toxigenicity of isolates from persistent carriers is consistent with the elevated antibody levels to classical SEs previously reported in persistent carriers, supporting the hypothesis that superantigen production in the nasal cavity may enhance colonisation.
Literature
1.
go back to reference Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5:751–762CrossRefPubMed Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5:751–762CrossRefPubMed
2.
go back to reference van Belkum A, Verkaik NJ, de Vogel CP, Boelens HA, Verveer J, Nouwen JL, Verbrugh HA, Wertheim HFL (2009) Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 199:1820–1826CrossRefPubMed van Belkum A, Verkaik NJ, de Vogel CP, Boelens HA, Verveer J, Nouwen JL, Verbrugh HA, Wertheim HFL (2009) Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 199:1820–1826CrossRefPubMed
3.
go back to reference Colque-Navarro P, Jacobsson G, Andersson R, Flock JI, Möllby R (2010) Levels of antibody against 11 Staphylococcus aureus antigens in a healthy population. Clin Vaccine Immunol 17:1117–1123PubMedCentralCrossRefPubMed Colque-Navarro P, Jacobsson G, Andersson R, Flock JI, Möllby R (2010) Levels of antibody against 11 Staphylococcus aureus antigens in a healthy population. Clin Vaccine Immunol 17:1117–1123PubMedCentralCrossRefPubMed
4.
go back to reference Kolata J, Bode LG, Holtfreter S, Steil L, Kusch H, Holtfreter B, Albrecht D, Hecker M, Engelmann S, van Belkum A, Völker U, Bröker BM (2011) Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11:3914–3927CrossRefPubMed Kolata J, Bode LG, Holtfreter S, Steil L, Kusch H, Holtfreter B, Albrecht D, Hecker M, Engelmann S, van Belkum A, Völker U, Bröker BM (2011) Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11:3914–3927CrossRefPubMed
5.
go back to reference Burian M, Grumann D, Holtfreter S, Wolz C, Goerke C, Bröker BM (2012) Expression of staphylococcal superantigens during nasal colonization is not sufficient to induce a systemic neutralizing antibody response in humans. Eur J Clin Microbiol Infect Dis 31:251–256CrossRefPubMed Burian M, Grumann D, Holtfreter S, Wolz C, Goerke C, Bröker BM (2012) Expression of staphylococcal superantigens during nasal colonization is not sufficient to induce a systemic neutralizing antibody response in humans. Eur J Clin Microbiol Infect Dis 31:251–256CrossRefPubMed
6.
go back to reference Holtfreter S, Roschack K, Eichler P, Eske K, Holtfreter B, Kohler C, Engelmann S, Hecker M, Greinacher A, Broker BM (2006) Staphylococcus aureus carriers neutralize superantigens by antibodies specific for their colonizing strain: a potential explanation for their improved prognosis in severe sepsis. J Infect Dis 193:1275–1278CrossRefPubMed Holtfreter S, Roschack K, Eichler P, Eske K, Holtfreter B, Kohler C, Engelmann S, Hecker M, Greinacher A, Broker BM (2006) Staphylococcus aureus carriers neutralize superantigens by antibodies specific for their colonizing strain: a potential explanation for their improved prognosis in severe sepsis. J Infect Dis 193:1275–1278CrossRefPubMed
7.
go back to reference Harrison LM, Morris JA, Bishop LA, Lauder RM, Taylor CA, Telford DR (2004) Detection of specific antibodies in cord blood, infant and maternal saliva and breast milk to staphylococcal toxins implicated in sudden infant death syndrome (SIDS). FEMS Immunol Med Microbiol 42:94–104CrossRefPubMed Harrison LM, Morris JA, Bishop LA, Lauder RM, Taylor CA, Telford DR (2004) Detection of specific antibodies in cord blood, infant and maternal saliva and breast milk to staphylococcal toxins implicated in sudden infant death syndrome (SIDS). FEMS Immunol Med Microbiol 42:94–104CrossRefPubMed
8.
go back to reference Holtfreter S, Nguyen TT, Wertheim H, Steil L, Kusch H, Truong QP, Engelmann S, Hecker M, Völker U, van Belkum A, Bröker BM (2009) Human immune proteome in experimental colonization with Staphylococcus aureus. Clin Vaccine Immunol 16:1607–1614PubMedCentralCrossRefPubMed Holtfreter S, Nguyen TT, Wertheim H, Steil L, Kusch H, Truong QP, Engelmann S, Hecker M, Völker U, van Belkum A, Bröker BM (2009) Human immune proteome in experimental colonization with Staphylococcus aureus. Clin Vaccine Immunol 16:1607–1614PubMedCentralCrossRefPubMed
9.
go back to reference van Belkum A, Melles DC, Nouwen J, Van Leeuwen WB, Van Wamel W, Vos MC, Wertheim HF, Verbrugh HA (2009) Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect Genet Evol 9:32–47CrossRefPubMed van Belkum A, Melles DC, Nouwen J, Van Leeuwen WB, Van Wamel W, Vos MC, Wertheim HF, Verbrugh HA (2009) Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect Genet Evol 9:32–47CrossRefPubMed
10.
go back to reference Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G (2001) egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166:669–677CrossRefPubMed Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G (2001) egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166:669–677CrossRefPubMed
11.
go back to reference Holtfreter S, Kolata J, Bröker BM (2010) Towards the immune proteome of Staphylococcus aureus - The anti-S. aureus antibody response. Int J Med Microbiol 300:176–192CrossRefPubMed Holtfreter S, Kolata J, Bröker BM (2010) Towards the immune proteome of Staphylococcus aureus - The anti-S. aureus antibody response. Int J Med Microbiol 300:176–192CrossRefPubMed
12.
go back to reference Omoe K, Hu DL, Ono HK, Shimizu S, Takahashi-Omoe H, Nakane A, Uchiyama T, Shinagawa K, Imanishi K (2013) Emetic potentials of newly identified staphylococcal enterotoxin-like toxins. Infect Immun 81:3627–3631PubMedCentralCrossRefPubMed Omoe K, Hu DL, Ono HK, Shimizu S, Takahashi-Omoe H, Nakane A, Uchiyama T, Shinagawa K, Imanishi K (2013) Emetic potentials of newly identified staphylococcal enterotoxin-like toxins. Infect Immun 81:3627–3631PubMedCentralCrossRefPubMed
13.
go back to reference Wattinger L, Stephan R, Layer F, Johler S (2012) Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections. Eur J Clin Microbiol Infect Dis 31:455–464CrossRefPubMed Wattinger L, Stephan R, Layer F, Johler S (2012) Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections. Eur J Clin Microbiol Infect Dis 31:455–464CrossRefPubMed
14.
go back to reference Argudín MA, Argumosa V, Mendoza MC, Guerra B, Rodicio MR (2013) Population structure and exotoxin gene content of methicillin-susceptible Staphylococcus aureus from Spanish healthy carriers. Microb Pathog 54:26–33CrossRefPubMed Argudín MA, Argumosa V, Mendoza MC, Guerra B, Rodicio MR (2013) Population structure and exotoxin gene content of methicillin-susceptible Staphylococcus aureus from Spanish healthy carriers. Microb Pathog 54:26–33CrossRefPubMed
15.
go back to reference Chiang YC, Liao WW, Fan CM, Pai WY, Chiou CS, Tsen HY (2008) PCR detection of staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 121:66–73CrossRefPubMed Chiang YC, Liao WW, Fan CM, Pai WY, Chiou CS, Tsen HY (2008) PCR detection of staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 121:66–73CrossRefPubMed
16.
go back to reference Ho J, Boost MV, O’Donoghue MM (2014) Sustainable reduction of nasal colonization and hand contamination with Staphylococcus aureus in food handlers, 2002–2011. Epidemiol Infect 143:1751–1760CrossRefPubMed Ho J, Boost MV, O’Donoghue MM (2014) Sustainable reduction of nasal colonization and hand contamination with Staphylococcus aureus in food handlers, 2002–2011. Epidemiol Infect 143:1751–1760CrossRefPubMed
17.
go back to reference Mehrotra M, Wang G, Johnson WM (2000) Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 38:1032–1035PubMedCentralPubMed Mehrotra M, Wang G, Johnson WM (2000) Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 38:1032–1035PubMedCentralPubMed
18.
go back to reference Monday SR, Bohach GA (1999) Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol 37:3411–3414PubMedCentralPubMed Monday SR, Bohach GA (1999) Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol 37:3411–3414PubMedCentralPubMed
19.
go back to reference Ono HK, Omoe K, Imanishi K, Iwakabe Y, Hu DL, Kato H, Saito N, Nakane A, Uchiyama T, Shinagawa K (2008) Identification and characterization of two novel staphylococcal enterotoxins, types S and T. Infect Immun 76:4999–5005PubMedCentralCrossRefPubMed Ono HK, Omoe K, Imanishi K, Iwakabe Y, Hu DL, Kato H, Saito N, Nakane A, Uchiyama T, Shinagawa K (2008) Identification and characterization of two novel staphylococcal enterotoxins, types S and T. Infect Immun 76:4999–5005PubMedCentralCrossRefPubMed
20.
go back to reference Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41:5442–5448 Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41:5442–5448
21.
go back to reference van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M; European Society of Clinical Microbiology and Infectious Diseases (ESCMID) Study Group on Epidemiological Markers (ESGEM) (2007) Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13(Suppl 3):1–46CrossRefPubMed van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M; European Society of Clinical Microbiology and Infectious Diseases (ESCMID) Study Group on Epidemiological Markers (ESGEM) (2007) Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13(Suppl 3):1–46CrossRefPubMed
22.
go back to reference Udo EE, Al-Mufti S, Albert MJ (2009) The prevalence of antimicrobial resistance and carriage of virulence genes in Staphylococcus aureus isolated from food handlers in Kuwait city restaurants. BMC Res Notes 2:108PubMedCentralCrossRefPubMed Udo EE, Al-Mufti S, Albert MJ (2009) The prevalence of antimicrobial resistance and carriage of virulence genes in Staphylococcus aureus isolated from food handlers in Kuwait city restaurants. BMC Res Notes 2:108PubMedCentralCrossRefPubMed
23.
go back to reference Monecke S, Luedicke C, Slickers P, Ehricht R (2009) Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis 28:1159–1165CrossRefPubMed Monecke S, Luedicke C, Slickers P, Ehricht R (2009) Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis 28:1159–1165CrossRefPubMed
24.
go back to reference Holtfreter S, Bauer K, Thomas D, Feig C, Lorenz V, Roschack K, Friebe E, Selleng K, Lövenich S, Greve T, Greinacher A, Panzig B, Engelmann S, Lina G, Bröker BM (2004) egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect Immun 72:4061–4071PubMedCentralCrossRefPubMed Holtfreter S, Bauer K, Thomas D, Feig C, Lorenz V, Roschack K, Friebe E, Selleng K, Lövenich S, Greve T, Greinacher A, Panzig B, Engelmann S, Lina G, Bröker BM (2004) egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect Immun 72:4061–4071PubMedCentralCrossRefPubMed
25.
go back to reference Derzelle S, Dilasser F, Duquenne M, Deperrois V (2009) Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 26:896–904CrossRefPubMed Derzelle S, Dilasser F, Duquenne M, Deperrois V (2009) Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 26:896–904CrossRefPubMed
26.
go back to reference Machuca MA, Sosa LM, González CI (2013) Molecular typing and virulence characteristic of methicillin-resistant Staphylococcus aureus isolates from pediatric patients in Bucaramanga, Colombia. PLoS One 8(8):e73434PubMedCentralCrossRefPubMed Machuca MA, Sosa LM, González CI (2013) Molecular typing and virulence characteristic of methicillin-resistant Staphylococcus aureus isolates from pediatric patients in Bucaramanga, Colombia. PLoS One 8(8):e73434PubMedCentralCrossRefPubMed
27.
go back to reference Climo MW, Sepkowitz KA, Zuccotti G, Fraser VJ, Warren DK, Perl TM, Speck K, Jernigan JA, Robles JR, Wong ES (2009) The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial. Crit Care Med 37:1858–1865CrossRefPubMed Climo MW, Sepkowitz KA, Zuccotti G, Fraser VJ, Warren DK, Perl TM, Speck K, Jernigan JA, Robles JR, Wong ES (2009) The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial. Crit Care Med 37:1858–1865CrossRefPubMed
28.
go back to reference David MZ, Siegel JD, Henderson J, Leos G, Lo K, Iwuora J, Porsa E, Schumm LP, Boyle-Vavra S, Daum RS (2014) A randomized, controlled trial of chlorhexidine-soaked cloths to reduce methicillin-resistant and methicillin-susceptible Staphylococcus aureus carriage prevalence in an urban jail. Infect Control Hosp Epidemiol 35:1466–1473CrossRefPubMed David MZ, Siegel JD, Henderson J, Leos G, Lo K, Iwuora J, Porsa E, Schumm LP, Boyle-Vavra S, Daum RS (2014) A randomized, controlled trial of chlorhexidine-soaked cloths to reduce methicillin-resistant and methicillin-susceptible Staphylococcus aureus carriage prevalence in an urban jail. Infect Control Hosp Epidemiol 35:1466–1473CrossRefPubMed
Metadata
Title
Prevalence of enterotoxin genes in Staphylococcus aureus colonising food handlers: does nasal carriage status matter?
Authors
J. Ho
M. Boost
M. O’Donoghue
Publication date
01-11-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 11/2015
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-015-2465-z

Other articles of this Issue 11/2015

European Journal of Clinical Microbiology & Infectious Diseases 11/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.