On 6 June 2017, the World Health Organization (WHO) published updates to its ‘Essential Medicines List’ (EML). Read more here.

Extended deadline (from 1 July to 31 July) 2017 for call to submit papers on effectiveness and cost-effectiveness of screening and prevention of infectious diseases among newly arrived migrants in Europe. Read more here.

Eurosurveillance is on the updated list of the Directory of Open Access Journals and in the SHERPA/RoMEO database. Read more here.

Follow Eurosurveillance on Twitter: @Eurosurveillanc

In this issue

Home Eurosurveillance Edition  2015: Volume 20/ Issue 45 Article 2
Back to Table of Contents
Previous Download (pdf)

Eurosurveillance, Volume 20, Issue 45, 12 November 2015
Surveillance and outbreak report
Mossong, Decruyenaere, Moris, Ragimbeau, Olinger, Johler, Perrin, Hau, and Weicherding: Investigation of a staphylococcal food poisoning outbreak combining case–control, traditional typing and whole genome sequencing methods, Luxembourg, June 2014

+ Author affiliations

Citation style for this article: Mossong J, Decruyenaere F, Moris G, Ragimbeau C, Olinger CM, Johler S, Perrin M, Hau P, Weicherding P. Investigation of a staphylococcal food poisoning outbreak combining case–control, traditional typing and whole genome sequencing methods, Luxembourg, June 2014. Euro Surveill. 2015;20(45):pii=30059. DOI:

Received:24 November 2014; Accepted:02 July 2015


Food poisoning caused by enterotoxigenic Staphylococcus aureus is one of the most common foodborne diseases [1]. In France, which has a long-established foodborne disease surveillance system able to detect fairly rare events [2], staphylococcal food poisoning (SFP) has ranked in recent years as the first cause of foodborne outbreaks: of 1,288 reported foodborne outbreaks in 2012, 300 (23%) were due to SFP [3]. SFPs are thought to be under-reported for several reasons. First, because of the short duration of symptoms, only an estimated 10% of SFP patients visit a hospital [4]. Even if patients seek medical care, the physician often does not deem a stool analysis necessary. If a stool analysis is performed, the microbiological routine procedures often do not include testing for the presence of enterotoxigenic S. aureus unless specifically requested by the physician [5]. In addition, staphylococcal enterotoxin (SE) is highly stable and heat-resistant. Although the bacteria may have been inactivated by heating the food prior to consumption and can therefore be isolated neither from food nor the stool of the patient, the highly stable enterotoxins preformed by S. aureus in the food may still be emetically active [6].

In contrast to most other gastrointestinal infections, the onset of SFP symptoms is very rapid, usually within a few hours after ingestion of the contaminated food. The median incubation period of aetiologically confirmed SFP outbreaks occurring in the United States between 1998 and 2008 was estimated to be four hours (5–95 percentile: two to seven hours) [7]. Symptoms in cases in these outbreaks typically included abdominal cramps (72%), vomiting (87%), and diarrhoea (89%). Fever (9%) was infrequently reported. The median duration of illness was 15 hours (5–95 percentile: 4–60 hours) [7].

Here, we report a SFP outbreak that occurred in a buffet restaurant at an international show-jumping event in Luxembourg in June 2014. A total of 31 persons had to be transferred by ambulance from the event site to emergency departments of three local hospitals. We describe findings of the ensuing epidemiological case–control study, the microbiological contamination of food samples, and colonisation by S. aureus of catering employees at the event. In particular, we characterised the S. aureus isolates from patients, food items obtained from the buffet, and food handlers using traditional typing methods (PCR, spa-typing, and multilocus variable-number tandem repeat analysis (MLVA)), as well as whole genome sequencing.

The event

From 12 to 15 June 2014, an equestrian show-jumping event with approximately 140 participating international athletes and 300 horses took place in Luxembourg. Approximately one to three hours after eating a buffet lunch in the tented VIP restaurant on 12 June, 11 persons with symptoms of vomiting, diarrhoea, and prostration were taken by ambulance to the emergency departments of two hospitals where they received parenteral fluids. The official health inspection service was informed immediately of the incident and microbiological analysis of stool samples from hospitalised patients was ordered. Official food safety inspectors proceeded immediately to take samples from remaining buffet items for microbiological analysis. An inspection of the professional caterer’s onsite restaurant and offsite kitchen did not reveal any major food safety deficiencies as specified in regulation (EC) 852/2004. The next morning, on 13 June, local newspapers announced salmon tartare as a potential culprit. A few hours after having the buffet lunch in the VIP restaurant on 13 June, a further 20 persons fell ill with the same symptoms and were transferred by ambulance to hospital emergency departments. The event organiser stopped serving any prepared meals for the remainder of the event. On 14 and 15 June, there were no further reports of gastrointestinal illness related to the event. While approximately 150-200 persons were estimated to have consumed the buffet lunch in the VIP restaurant on both days and a total of 31 persons were admitted to hospital emergency departments over the two days, the exact number of affected persons is unknown. There were no reports of illness among those people who ate at the other food-serving premises at the event: a non-VIP lunch buffet operated by the same caterer but with different menus, and a barbecue stall hosted by non-professional club members.


Microbiological examination of stool samples

Culture of stool samples for bacterial pathogens (including Salmonella, Campylobacter and verotoxigenic Escherichia coli) conducted in three hospital laboratories revealed the presence of S. aureus in ten patients and Enterococcus in one patient. Isolates of S. aureus were immediately referred to the National Health Laboratory for further molecular characterisation.

Case-control study

Following their recovery from illness and after the food samples had been analysed, eight cases who had been admitted to emergency care were contacted by telephone to get initial information on potential food exposures. All food items and symptoms reported by cases were included in a final questionnaire administered by telephone to 22 cases and 21 controls. Cases were defined as persons with sudden gastrointestinal illness (at least one symptom: vomiting, diarrhoea, abdominal cramps or nausea) who had eaten buffet lunch at the VIP restaurant on 12 or 13 June. Controls were defined as persons who had eaten buffet lunch at the VIP restaurant on 12 or 13 June, without any gastrointestinal symptoms. Non-hospitalised cases and controls were contacted using information provided by the event organiser.

Testing of food samples

Food samples were tested by accredited methods for aerobic plate count, E. coli, coagulase-positive staphylococci (ISO 6888-2:1999), Salmonella, and Bacillus cereus. The salmon tartare and floating island dessert samples were additionally tested for Listeria monocytogenes.

Staphylococcal carriage study among caterer’s employees

Following the detection of S. aureus in patients, a staphylococcal carriage study was conducted on 19 and 20 June among the caterer’s employees who worked in the onsite restaurant or in the offsite kitchen where buffet items were prepared, including the slicing of ham. Catering employees screened included waiters, cooks, and other kitchen staff. Throat and nose swabs were taken by doctors and sent the same day to the laboratory where they were streaked onto selective Chapman media (reference 51053, BioMérieux, Marcy l’Etoile, France).

Characterisation of S. aureus isolates and whole genome sequencing

Isolates of S. aureus obtained from patients, food, and catering employees were confirmed by MALDI-TOF mass spectrometry (Bruker, Brussels, Belgium). Confirmed isolates of S. aureus were further characterised for the presence of nuc, mecA, toxic shock syndrome toxin 1 (TSST-1), and Panton-Valentine leukocidine (PVL) [8] as well as genes coding for staphylococcal enterotoxins A (sea), B, C, D E, H, I, and J [9]. Isolates exhibiting sea were further characterised by sequencing the PCR products and compared to strains containing allelic sea variants FRI100, FRI287A, and N315. In addition, isolates were subjected to spa-typing [8] and MLVA typing [10]. Whole genome sequencing of isolates was performed on a Miseq Desktop Sequencer using the Nextera DNA sample preparation kit (Illumina, Eindhoven, The Netherlands) with an average coverage of 59 fold (range 27-140 fold). Antimicrobial resistance genes, virulence factors and multi-locus sequence types (MLST) were determined by submitting the raw read files to public webserver tools hosted by the Center for Genomic Epidemiology in Denmark [11-13]. After sequencing, whole genome MLST+ was conducted using the Seqsphere+ v2.3 pipeline (Ridom, Münster, Germany). Briefly, after trimming reads until the average quality was 30 in a window of 30 bases, the trimmed reads were mapped to the reference genome NC_002951.2 and the allelic profiles of 1,878 target genes were determined based on the MLST+ scheme developed previously [14]. Final phylogenetic analysis was based on 10 patient isolates, 6 food isolates, 22 carrier isolates of members of staff, and an isolate with spa-type t024 from an unrelated Swiss outbreak in 2010. The whole genome reads were deposited at the European Nucleotide Archive (study accession no. PRJEB7847). For the purpose of this study, we use the terminology ‘genotype’ to denote the combined typing results of MLST, spa- and MLVA typing.


Fifteen (48%) of the 31 patients admitted by ambulance to emergency care were women. The median age was 35 years (range 14–58 years). Three patients were catering staff at the event. Six patients were non-residents of Luxembourg. Information on clinical symptoms was available for 22 of the patients and included diarrhoea (20 patients), nausea (19 patients), cramps (19 patients) and vomiting (17 patients). All admitted patients were discharged within 48 hours. All 10 isolates obtained from patients’ stool samples represented the same genotype (MLST sequence type (ST)-8, spa-type t024, MLVA-type 4698), possessed genes encoding sea allele FRI100 and conferring penicillin resistance mediated by blaZ.

Results from the analytical epidemiological case–control study (Table) implicated consumption of pasta salad with pesto as the most likely vehicle of SFP. Eighteen of 22 cases reported eating this food item compared to 3 of 21 controls (p<0.0001). All 14 interviewed cases who had been hospitalised reported eating the pasta salad with pesto. Unfortunately, there were no leftovers of the pasta salad with pesto when sampling was taking place and so this dish was not available for microbiological testing. Eating cured ham or salmon tartare were not statistically significant risk factors (p=0.45). One interviewed patient reported not having eaten ham at the buffet for religious reasons.


Results from analytical case–control study of food exposures, staphylococcal food poisoning outbreak, Luxembourg, June 2014

Food item at VIP buffet Cases N (%) Controls N (%) Odds ratio p value
Cooked ham 10 (45%) 6 (27%) 2.08 (0.50–9.04) 0.25
Cured ham 13 (59%) 10 (45%) 1.59 (0.41–6.28) 0.45
Grilled shrimps 12 (55%) 8 (36%) 1.95 (0.49–7.84) 0.28
Lamb 13 (59%) 11 (50%) 1.31 (0.33–5.18) 0.66
Melon 13 (59%) 12 (55%) 1.08 (0.27–4.30) 0.90
Panna cotta 13 (59%) 9 (41%) 1.93 (0.49–7.68) 0.29
Pesto pasta salad 18 (82%) 3 (14%) 27 (4.35–195.43) <0.0001
Potato gratin 15 (68%) 13 (59%) 1.32 (0.31–5.59) 0.67
Potato salad 10 (45%) 11 (50%) 0.76 (0.19–2.94) 0.65
Prawns 3 (14%) 1 (5%) 3.16 (0.22–173.90) 0.32
Raw vegetables 13 (59%) 11 (50%) 1.31 (0.33–5.18) 0.66
Risotto 12 (55%) 9 (41%) 1.6 (0.41–6.31) 0.44
Ruccola salad 10 (45%) 10 (45%) 0.92 (0.24–3.57) 0.89
Salmon tartare 3 (14%) 2 (9%) 1.5 (0.15–19.7) 0.67

Food samples

Isolates of S. aureus with a genotype identical to patient isolates (MLST ST-8, spa-type t024, MLVA-type 4698) were detected in cured ham samples (range <40–5,200 colony-forming units (CFU)/g and shiitake mushrooms (<40 CFU/g) sampled at the event site and in cured ham samples (enumeration range <40–120 CFU/g) obtained at the offsite catering kitchen where the ham was sliced and stored (Figure). Non-enterotoxigenic isolates of S. aureus with a different genotype to patient isolates were found in cooked asparagus (<40 CFU/g, MLST ST-398, spa-type t571, MLVA type 1039), the floating island dessert (<40 CFU/g, MLST ST-398, spa-type t1184, MLVA-type 567) and several samples of cooked ham (range 50–320 CFU/g, MLST ST-398, spa-type t571, MLVA-type 4789). Unsliced complete legs of cured and cooked hams obtained from the supplying butcher were negative for S. aureus. All 18 food items sampled from the event buffet were negative for Salmonella and E. coli. One food item (cooked asparagus) was positive for presumptive Bacillus cereus (840 CFU/g).


Clonal relationship between patient, food, and catering staff isolates, staphylococcal food poisoning outbreak, Luxembourg, June 2014


A phylogenetic dendrogram (neighbour joining tree) was generated for 39 Staphylococcus aureus isolates based on the allelic profiles of 1,625 available of 1,878 queried MLST+ target genes. The scale bars indicate the number of differing alleles comprising the calculated distance. The colours represent the origin of outbreak-related strains (orange: stool samples from hospitalised patients; blue: food samples; green: throat or nose samples from colonised staff members). The genotype column shows the combined data of multilocus sequence typing (prefix ST), spa-typing (prefix t), and MLVA typing (prefix m).

The pasta salad with pesto could not be sampled during food inspection, as there were no leftovers from this dish. The primary ingredients used to make the pesto sauce for the pasta salad (fresh basil, hard cheese, and pine nuts) were all negative for S. aureus.

Staphylococcal carriage study

Thirty-eight of the 49 catering employees at the event were screened for nasal/throat carriage of S. aureus. Median age of the screened employees was 32.5 years (range 17–50 years), and 11 were women. Twenty-two employees were found to be colonised by S. aureus: three staff members were colonised by strains identical to those found in patients (Figure). Another four employees were colonised by S. aureus isolates exhibiting sea, but a different genotype than the outbreak strain. None of the seven employees colonised by isolates exhibiting sea reported wounds or gastrointestinal disease prior to the event. Overall, 17 different genotypes were observed among the 22 colonised employees. None of the isolates in food, patients, or catering employees were meticillin-resistant or exhibited pvl.

Whole genome sequencing

The whole genome phylogeny (Figure), as determined by 1,625 of 1,878 MLST and MLST+ target genes that were present in all 39 isolates, clearly delineated the outbreak isolates. S. aureus isolates found in 10 patients were identical to those isolated from cured ham, shiitake mushrooms and from three catering employees. Interestingly, the Luxembourg outbreak strain had 347 allele differences with a strain that led to the intoxication of 27 boy scouts in Switzerland in 2010, although both strains share a common spa-type t024 [15]. Two of the three food isolates which differed from the outbreak strain were also observed among catering employees. These belonged to livestock-associated sequence type ST398 with spa-types t571 or t1184.


Studies of foodborne outbreaks, in which enterotoxigenic isolates were detected in patients, food, and food handlers, are rare [16-18]. Our report shows that, even in the era of whole genome sequencing, public health investigations of foodborne outbreaks remain very dependent on classical case–control investigations for interpretation of events. Whereas initial microbiological typing results suggested cured ham as the main vehicle for the intoxication, the case–control study clearly identified the pasta salad with pesto as the most likely source, which was no longer available for microbiological testing.

In our outbreak, there was good evidence that the pathogen responsible for the outbreak was S. aureus, because identical enterotoxigenic strains of S. aureus with a common spa-type but rare MLVA type were recovered from the stools of 10 hospitalised cases. Because three catering employees were colonised by a strain with the same genotype, it is likely that at least one of them may represent the source of food contamination, either via manual contact or through respiratory secretions [19]. However, because catering employees were screened a week after the outbreak, it cannot also be ruled out that some staff members became colonised only during or after the event [20].

One of the probable factors contributing to the outbreak may have been the unusually hot weather for the season, with maximum temperatures ranging between 25 °C and 32 °C during the week preceding the event, compared with a historical average of 21 °C. The food safety inspection at the catering facility revealed that a fridge had stopped working properly a few days prior to the event, although the catering staff denied using this fridge to store any of the dishes. The pasta salad with pesto was reported to have been pre-cooked and sealed into plastic bags in 2 kg portions, and then cooled down in a fast refrigeration unit. Nevertheless, the fact that S. aureus was detected in several dishes including cured and cooked ham, at concentrations up to 5,200 CFU/g, suggests that the cold chain before or during the event was interrupted to allow sufficient microbial growth during or following food manipulation.

A major limitation of our study is that the food item identified by the case–control study, pasta salad with pesto, was no longer available for testing and thus there is no microbiological evidence that the pasta salad with pesto was contaminated with the outbreak strain. However, matrices with similar biochemical properties like potato salad have been confirmed before as vehicles of SFP in France [21] and Switzerland [15]. In the latter case, a strain with identical spa type t024 and enterotoxin A FRI100 allele led to the intoxication of 27 boy scouts. The sea gene found in our outbreak strain is the dominant sea allele described in S. aureus isolates that are associated with food poisoning outbreaks worldwide [19,21-23] and in enterotoxigenic isolates recovered from food handlers [24].

The epidemiological results from our carriage study are consistent with previous findings in similar studies. Our finding of 58% carriers among food handlers concurs with longitudinal studies showing that approximately 20% of persons are persistent nasal carriers and an additional 30% are intermittent carriers of S. aureus [25]. The high genetic diversity among asymptomatic carriers was also observed in similar studies in Germany [26], Switzerland [27], and Bosnia [28]. Interestingly, we found meticillin-susceptible livestock–associated strains with ST398 spa type t571 and variants thereof in both catering employees and in food. Similar clones have recently emerged causing severe infections in neighbouring France and Belgium [29,30], while remaining rare in Germany [31].

Although WGS has been applied to meticillin-resistant S. aureus in hospital and long-term care settings [32-34] and to other foodborne pathogens [35,36], to our knowledge our study is the first to report WGS as a tool in a staphylococcal food poisoning outbreak. While WGS showed virtually identical groupings to MLVA, one major advantage of WGS is that it is a universal method applicable to any bacterial species and that it provides further data on the presence of genes encoding virulence and resistance factors.


We thank the hospital biologists Drs Cynthia Oxacelay, Nawfal Faik, and Alain Hakim, who provided us with the patient isolates and the occupational health service who took throat and nasal swab samples from the catering employees.

Conflict of interest

None declared.

Authors’ contributions

JM coordinated the various investigations, collated strains from different sources, constructed phylogenies, conducted the statistical analysis for the case–control study, and wrote the manuscript; FD conducted the classical genotyping including MLVA, spa typing and virulence factor detection by PCR; GM was responsible for the laboratory analysis of food items; CR and CO conducted the whole genome sequencing; CO assisted with bioinformatics and with preparing the figure; SJ provided reference material and assisted with interpretation; MP was responsible for the microbiological analysis of human strains; PH led the food inspection; PW was responsible for the public health response and the case–control data collection.


  1. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation.FEMS Microbiol Rev. 2012;36(4):815-36. .DOI: 10.1111/j.1574-6976.2011.00311.x PMID: 22091892

  2. Ostyn A, De Buyser ML, Guillier F, Groult J, Felix B, Salah S,  et al.  First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009. Euro Surveill. 2010;15(13).PMID: 20394711

  3. Institut de Veille Sanitaire (InVS). Surveillance des toxi-infections alimentaires collectives. Données de la déclaration obligatoire. [Surveillance of foodborne illness. Data from mandatory reporting]. Saint-Maurice, France: INVS; 2012. French. Available from:

  4. Holmberg SD, Blake PA. Staphylococcal food poisoning in the United States. New facts and old misconceptions.JAMA. 1984;251(4):487-9. .DOI: 10.1001/jama.1984.03340280037024 PMID: 6690814

  5. Cornaglia G, Courcol R, Herrmann J-L, Kahlmeter G, Peigue-Lafeuille H, Vila J, editors. European Manual of Clinical Microbiology. 1st ed. Basel: European Society for Clinical Microbiology and Infectious Diseases and Société Française de Microbiologie; 2012.

  6. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning.Genet Mol Res. 2003;2(1):63-76.PMID: 12917803

  7. Bennett SD, Walsh KA, Gould LH. Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus--United States, 1998-2008.Clin Infect Dis. 2013;57(3):425-33. .DOI: 10.1093/cid/cit244 PMID: 23592829

  8. Mossong J, Gelhausen E, Decruyenaere F, Devaux A, Perrin M, Even J,  et al.  Prevalence, risk factors and molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) colonization in residents of long-term care facilities in Luxembourg, 2010. Epidemiol Infect. 2013;141(6):1199-206. .DOI: 10.1017/S0950268812001999 PMID: 22953727

  9. Kwon NH, Kim SH, Park KT, Bae WK, Kim JY, Lim JY,  et al.  Application of extended single-reaction multiplex polymerase chain reaction for toxin typing of Staphylococcus aureus isolates in South Korea. Int J Food Microbiol. 2004;97(2):137-45. .DOI: 10.1016/j.ijfoodmicro.2004.04.014 PMID: 15541800

  10. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Santen-Verheuvel MG,  et al.  Multiple-locus variable number tandem repeat analysis of Staphylococcus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PLoS ONE. 2009;4(4):e5082. .DOI: 10.1371/journal.pone.0005082 PMID: 19343175

  11. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O,  et al.  Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4. .DOI: 10.1093/jac/dks261 PMID: 22782487

  12. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL,  et al.  Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355-61. .DOI: 10.1128/JCM.06094-11 PMID: 22238442

  13. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM,  et al.  Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501-10. .DOI: 10.1128/JCM.03617-13 PMID: 24574290

  14. Leopold SR, Goering RV, Witten A, Harmsen D, Mellmann A. Bacterial whole-genome sequencing revisited: portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes.J Clin Microbiol. 2014;52(7):2365-70. .DOI: 10.1128/JCM.00262-14 PMID: 24759713

  15. Johler S, Layer F, Stephan R. Comparison of virulence and antibiotic resistance genes of food poisoning outbreak isolates of Staphylococcus aureus with isolates obtained from bovine mastitis milk and pig carcasses.J Food Prot. 2011;74(11):1852-9. .DOI: 10.4315/0362-028X.JFP-11-192 PMID: 22054185

  16. Wei HL, Chiou CS. Molecular subtyping of Staphylococcus aureus from an outbreak associated with a food handler.Epidemiol Infect. 2002;128(1):15-20. .DOI: 10.1017/S0950268801006355 PMID: 11895086

  17. Schmid D, Gschiel E, Mann M, Huhulescu S, Ruppitsch W, Bohm G,  et al.  Outbreak of acute gastroenteritis in an Austrian boarding school, September 2006. Euro Surveill. 2007;12(3):224.PMID: 17439809

  18. Johler S, Tichaczek-Dischinger PS, Rau J, Sihto HM, Lehner A, Adam M,  et al.  Outbreak of Staphylococcal food poisoning due to SEA-producing Staphylococcus aureus. Foodborne Pathog Dis. 2013;10(9):777-81. .DOI: 10.1089/fpd.2013.1503 PMID: 23767854

  19. Argudín MA, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins.Toxins (Basel). 2010;2(7):1751-73. .DOI: 10.3390/toxins2071751 PMID: 22069659

  20. Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int. 2014;2014:827965.

  21. Kérouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A,  et al.  Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol. 2007;115(3):369-75. .DOI: 10.1016/j.ijfoodmicro.2006.10.050 PMID: 17306397

  22. Yan X, Wang B, Tao X, Hu Q, Cui Z, Zhang J,  et al.  Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China. Appl Environ Microbiol. 2012;78(18):6637-42. .DOI: 10.1128/AEM.01165-12 PMID: 22798367

  23. Veras JF, do Carmo LS, Tong LC, Shupp JW, Cummings C, Dos Santos DA,  et al.  A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. Int J Infect Dis. 2008;12(4):410-5. .DOI: 10.1016/j.ijid.2007.09.018 PMID: 18206412

  24. Argudín MA, Mendoza MC, González-Hevia MA, Bances M, Guerra B, Rodicio MR. Genotypes, exotoxin gene content, and antimicrobial resistance of Staphylococcus aureus strains recovered from foods and food handlers.Appl Environ Microbiol. 2012;78(8):2930-5. .DOI: 10.1128/AEM.07487-11 PMID: 22327598

  25. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA,  et al.  The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751-62. .DOI: 10.1016/S1473-3099(05)70295-4 PMID: 16310147

  26. Monecke S, Luedicke C, Slickers P, Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers.Eur J Clin Microbiol Infect Dis. 2009;28(9):1159-65. .DOI: 10.1007/s10096-009-0752-2 PMID: 19434432

  27. Wattinger L, Stephan R, Layer F, Johler S. Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections.Eur J Clin Microbiol Infect Dis. 2012;31(4):455-64. .DOI: 10.1007/s10096-011-1330-y PMID: 21761125

  28. Uzunović S, Ibrahimagic A, Kamberovic F, Rijnders MIA, Stobberingh EE. Molecular Characterization of Methicillin-Susceptible And Methicillin-Resistant Staphylococcus aureus in Food Handlers in Bosnia and Herzegovina.Open Infect Dis J. 2013;7(1):15-20. .DOI: 10.2174/1874279301307010015

  29. Brunel AS, Bañuls AL, Marchandin H, Bouzinbi N, Morquin D, Jumas-Bilak E,  et al.  Methicillin-sensitive Staphylococcus aureus CC398 in intensive care unit, France. Emerg Infect Dis. 2014;20(9):1511-5. .DOI: 10.3201/eid2009.130225 PMID: 25148514

  30. Vandendriessche S, Kadlec K, Schwarz S, Denis O. Methicillin-susceptible Staphylococcus aureus ST398-t571 harbouring the macrolide-lincosamide-streptogramin B resistance gene erm(T) in Belgian hospitals.J Antimicrob Chemother. 2011;66(11):2455-9. .DOI: 10.1093/jac/dkr348 PMID: 21868413

  31. Cuny C, Layer F, Köck R, Werner G, Witte W. Methicillin susceptible Staphylococcus aureus (MSSA) of clonal complex CC398, t571 from infections in humans are still rare in Germany.PLoS ONE. 2013;8(12):e83165. .DOI: 10.1371/journal.pone.0083165 PMID: 24367584

  32. Köser CU, Holden MT, Ellington MJ, Cartwright EJ, Brown NM, Ogilvy-Stuart AL,  et al.  Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med. 2012;366(24):2267-75. .DOI: 10.1056/NEJMoa1109910 PMID: 22693998

  33. Harris SR, Cartwright EJP, Török ME, Holden MTG, Brown NM, Ogilvy-Stuart AL,  et al.  Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis. 2013;13(2):130-6. .DOI: 10.1016/S1473-3099(12)70268-2 PMID: 23158674

  34. Price JR, Golubchik T, Cole K, Wilson DJ, Crook DW, Thwaites GE,  et al.  Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus in an intensive care unit. Clin Infect Dis. 2014;58(5):609-18. .DOI: 10.1093/cid/cit807 PMID: 24336829

  35. Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C, Kleta S,  et al.  Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011-2013. Clin Microbiol Infect. 2014;20(5):431-6. .DOI: 10.1111/1469-0691.12638 PMID: 24698214

  36. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A,  et al.  Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS ONE. 2011;6(7):e22751. .DOI: 10.1371/journal.pone.0022751 PMID: 21799941

Back to Table of Contents
Previous Download (pdf)

The publisher’s policy on data collection and use of cookies.

Disclaimer: The opinions expressed by authors contributing to Eurosurveillance do not necessarily reflect the opinions of the European Centre for Disease Prevention and Control (ECDC) or the editorial team or the institutions with which the authors are affiliated. Neither ECDC nor any person acting on behalf of ECDC is responsible for the use that might be made of the information in this journal. The information provided on the Eurosurveillance site is designed to support, not replace, the relationship that exists between a patient/site visitor and his/her physician. Our website does not host any form of commercial advertisement. Except where otherwise stated, all manuscripts published after 1 January 2016 will be published under the Creative Commons Attribution (CC BY) licence. You are free to share and adapt the material, but you must give appropriate credit, provide a link to the licence, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.

Eurosurveillance [ISSN] - ©2007-2016. All rights reserved

This website is certified by Health On the Net Foundation. Click to verify. This site complies with the HONcode standard for trustworthy health information:
verify here.