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Identifying risk factors for shiga toxin-producing Escherichia coli by payment information.
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PMID:  22261344     Owner:  NLM     Status:  MEDLINE    
Hendrik Wilking; Udo Götsch; Helma Meier; Detlef Thiele; Mona Askar; Manuel Dehnert; Christina Frank; Angelika Fruth; Gérard Krause; Rita Prager; Klaus Stark; Boris Böddinghaus; Oswald Bellinger; René Gottschalk
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Publication Detail:
Type:  Letter    
Journal Detail:
Title:  Emerging infectious diseases     Volume:  18     ISSN:  1080-6059     ISO Abbreviation:  Emerging Infect. Dis.     Publication Date:  2012 Jan 
Date Detail:
Created Date:  2012-01-20     Completed Date:  2012-05-15     Revised Date:  2013-06-26    
Medline Journal Info:
Nlm Unique ID:  9508155     Medline TA:  Emerg Infect Dis     Country:  United States    
Other Details:
Languages:  eng     Pagination:  169-70     Citation Subset:  IM    
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MeSH Terms
Contact Tracing / methods*
Disease Outbreaks
Food Microbiology*
Germany / epidemiology
Hemolytic-Uremic Syndrome / epidemiology*,  microbiology*
Middle Aged
Shiga-Toxigenic Escherichia coli / isolation & purification*
Young Adult

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): Emerg Infect Dis
Journal ID (publisher-id): EID
ISSN: 1080-6040
ISSN: 1080-6059
Publisher: Centers for Disease Control and Prevention
Article Information

Print publication date: Month: 1 Year: 2012
Volume: 18 Issue: 1
First Page: 169 Last Page: 170
ID: 3310115
PubMed Id: 22261344
Publisher Id: 11-1044
DOI: 10.3201/eid1801.111044

Identifying Risk Factors for Shiga Toxin–producing Escherichia coli by Payment Information Alternate Title:Risk Factors for STEC
Hendrik Wilking
Udo Götsch
Helma Meier
Detlef Thiele
Mona Askar
Manuel Dehnert
Christina Frank
Angelika Fruth
Gérard Krause
Rita Prager
Klaus Stark
Boris Böddinghaus
Oswald Bellinger
René Gottschalk
Robert Koch Institute, Berlin, Germany (H. Wilking, M. Askar, M. Dehnert, C. Frank, G. Krause, K. Stark);
Health Protection Authority, Frankfurt am Main, Germany (U. Götsch, B. Böddinghaus, O. Bellinger, R. Gottschalk);
Veterinary Service, Frankfurt am Main (H. Meier, D. Thiele);
Robert Koch Institute, Wernigerode, Germany (A. Fruth, R. Prager)
Correspondence: Address for correspondence: Hendrik Wilking, Robert Koch Institute, Department for Infectious Disease Epidemiology, DGZ-Ring 1, 13086 Berlin, Germany; email:

To the Editor: During May and June 2011, a large outbreak of hemolytic uremic syndrome (HUS) and diarrhea caused by Shiga toxin–producing Escherichia coli (STEC) occurred, centered on northern Germany (1,2). Early on, salads and raw vegetables were suspected to be food vehicles (3). Also in May, the staff department of a local company informed the Health Protection Authority in Frankfurt in southwestern Germany about the rapidly increasing number of patients with bloody diarrhea and HUS among employees at 2 company office sites. Both sites were served by cafeterias run by the same caterer. Main dishes were prepared in the cafeterias’ kitchens and differed between the 2 sites. However, in both cafeterias various fresh foods from a salad bar and fruits, desserts, and daily asparagus dishes originated from the caterer’s main kitchen. The salad bar included 30 items. Suspecting that this outbreak was linked to the one in northern Germany, we conducted an outbreak investigation to confirm the epidemiologic link to focus epidemiologic and traceback investigations.

A face-to-face survey among hospitalized employees and by email among all other employees was conducted, which included personal details, symptoms, and information about general food eaten at the cafeterias. We defined outbreak cases as infections in employees of the company at 1 of the 2 sites who by May 23, 2011, were either hospitalized with bloody diarrhea or HUS or who self-reported onset of bloody diarrhea from May 8 through May 23. A total of 320 persons responded to the survey, and 285 (89%) of 320 of the responders stated they used the cafeterias; 60 employees fulfilled our case definition. Case-patients’ median age was 33 years (range 22–60 years); 36 (60%) of 60 were female. Thirty case-patients were hospitalized; HUS developed in 18 (30%) (Figure A1). Disease onsets occurred over 9 days. Beginning and magnitude of the outbreak were not different between cafeteria locations. Bacteriologic diagnostics for 11 patients yielded results that are compatible with the outbreak strain (4).

We used billing data from the cafeterias’ obligatory cashless payment system to ascertain risk factors for disease. A nested case–control study design was chosen, limited to a fraction of the cohort to obtain rapid risk estimates. Exposures included were purchases of any fruit, salad bar item, dessert, or asparagus dish in either cafeteria from May 2 through May 13. On the basis of customer identification numbers, the caterer provided billing information for persons with early cases (n = 23). Controls were randomly chosen persons from the caterer’s database whose disease status was checked against the survey information (n = 30) and who did not report symptoms of diarrhea (nonbloody), vomiting, or nausea during the same period. Univariable logistic regression was performed.

In univariable analysis, salad bar purchases were highly associated with illness (odds ratio 5.19; 95% CI 1.28–21.03), and desserts, fruit, and asparagus dishes were not (Table). Three (9%) of the case-patients remained unexposed to salad bar items according to the payment system data. The analysis of main courses purchased in 1 cafeteria revealed that no such meal had been consumed by >5 (22%) of 23 case-patients. Beginning May 23, the cafeterias were closed for 1 week, and salad sales were suspended for a longer period. There were no additional cases.

These results and the identification of the same rare serotype of O104:H4 renders this a satellite outbreak to the larger outbreak in northern Germany, which is the largest outbreak in terms of HUS ever described worldwide. Sprouts are believed to be the food vehicle (5). Sprouts available in the Frankfurt cafeteria salad bars were traced back to a producer of fenugreek sprouts, which appear to be the common source of primary cases in the entire outbreak (5). Sprout consumption could not be studied directly in Frankfurt because of the intense media attention on the sprout hypothesis once it had been announced. Also, it was thought that too much time had passed to successfully recall actually selected salad bar items consumed a few weeks previous.

Cafeteria billing information allowed for a rapid investigation while avoiding exposure misclassification attributable to ill-remembered food purchases (6). Using data sources independent of individual memory is quite useful. In previous studies, similar tools were successfully applied for the detection of outbreak vehicles. Credit card information was used during an investigation on STEC in beef sausages in Denmark (7), supermarket purchase records for STEC in Iceland (8), and grocery store loyalty card records for cyclosporiasis in Canada (9). Shopper card information was used in the United States in an outbreak of Salmonella enterica serovar Montevideo (10). However, billing information also could have introduced exposure misclassification, e.g., purchased food that was left uneaten or brought for colleagues. Analysis on ingredient level is often not possible. This study emphasizes the need for recall-independent investigation methods. In settings where such methods are available, they should be exploited early and relevant data saved from routine deletion.


Suggested citation for this article: Wilking H, Götsch U, Meier H, Thiele D, Askar M, Dehnert M, et al. Identifying risk factors for Shiga toxin–producing Escherichia coli by payment information [letter]. Emerg Infect Dis [serial on the Internet] 2012 Jan [date cited].


We are grateful to the caterer, the employees, and the company management for their cooperation. We thank each member of the Robert Koch Institute HUS Investigation Team for their indispensable work and the coordinators of the German Postgraduate Training for Applied Epidemiology and the European Programme for Intervention Epidemiology Training for their help.

1. . FrankC, WerberD, CramerJ, AskarM, FaberM, an der HeidenM, et al. Epidemic profile of Shiga-toxin–producing Escherichia coli O104:H4 outbreak in Germany.N Engl J Med. Year: 2011;365:1771–8010.1056/NEJMoa110648321696328
2. . WadlM, RieckT, NachtnebelM, GreutélaersB, An der HeidenM, AltmannD, et al. Enhanced surveillance during a large outbreak of bloody diarrhoea and haemolytic uraemic syndrome caused by Shiga toxin/verotoxin–producing Escherichia coli in Germany, May to June 2011. Euro Surveill. Year: 2011;16:pii:19893.
3. . FrankC, FaberM, AskarM, BernardH, FruthA, GilsdorfA, et al. Large and ongoing outbreak of haemolytic uraemic syndrome, Germany, May 2011. Euro Surveill. Year: 2011;16:pii:19878.
4. . BielaszewskaM, MellmannA, ZhangW, KöckR, FruthA, BauwensA, et al. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study.Lancet Infect Dis. Year: 2011;11:671–621703928
5. . BuchholzU, BernardH, WerberD, BöhmerMM, RemschmidtC, WilkingH, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts.N Engl J Med. Year: 2011;365:1763–7010.1056/NEJMoa110648222029753
6. . DeckerMD, BoothAL, DeweyMJ, FrickerRS, HutchesonRH, SchaffnerWValidity of food consumption histories in a foodborne outbreak investigation.Am J Epidemiol. Year: 1986;124:859–633766519
7. . EthelbergS, SmithB, TorpdahlM, LisbyM, BoelJ, JensenT, et al. Outbreak of non-O157 Shiga toxin–producing Escherichia coli infection from consumption of beef sausage.Clin Infect Dis. Year: 2009;48:e78–8110.1086/59750219272017
8. . SigmundsdottirG, AtladottirA, HardardottirH, GudmundsdottirE, GeirsdottirM, BriemH. STEC O157 outbreak in Iceland, September-October 2007. Euro Surveill. Year: 2007;12(11):E071101.2.
9. . ShahL, MacDougallL, EllisA, OngC, ShyngS, LeBlancLChallenges of investigating community outbreaks of cyclosporiasis, British Columbia, Canada.Emerg Infect Dis. Year: 2009;15:1286–810.3201/eid1508.08158519751593
10. . Centers for Disease Control and PreventionSalmonella montevideo infections associated with salami products made with contaminated imported black and red pepper—United States, July 2009–April 2010.MMWR Morb Mortal Wkly Rep. Year: 2010;59:1647–5021178949


[Figure ID: FA.1]
Figure A1 

Patients with Shiga toxin–producing Escherichia coli/hemolytic uremic syndrome (STEC/HUS) by onset of diarrhea and cafeteria visit (location A or B) during STEC/HUS outbreak at a company in Frankfurt, Germany, 2011 (N = 51). NA, visited both cafeterias or specification was missing.

[TableWrap ID: T1] Table  Univariable analysis of risk factors for bloody diarrhea among users of 2 cafeterias in Frankfurt, Germany, 2011
Risk factor No. case-patients exposed/ total no. (%) No. controls exposed/ total no. (%) Univariable analysis*
Odds ratio (95% CI) p value
Salad bar 20/23 (87) 16/30 (53) 5.83 (1.42–23.88) 0.014
Dessert 16/23 (70) 18/30 (60) 1.52 (0.48–4.81) 0.473
Fruits 5/23 (22) 10/30 (33) 0.53 (0.15–1.81) 0.312
Asparagus dish 7/23 (30) 11/30 (37) 0.76 (0.24–2.41) 0.635
Female sex 16/23 (70) 15/30 (50) 2.28 (0.73–7.15) 0.155
Age, y
<30 12/23 (52) 6/30 (20) 2.80 (0.62–12.66) 0.181
30–<40 5/23 (22) 7/30 (23) Reference Reference
40–<50 4/23 (17) 13/30 (43) 0.43 (0.09–2.14) 0.303
>50 2/23 (9) 4/30 (13) 0.70 (0.09–5.43) 0.733

*Estimates in a multivariable model remained virtually unchanged.

Article Categories:
  • Letters to the Editor
Article Categories:
  • Letter

Keywords: Keywords: foodborne diseases, bacteria, Shiga-toxigenic, Escherichia coli, Shiga toxin–producing disease outbreaks, STEC, hemolytic-uremic syndrome, case–control studies, enteric infections.

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