Skip to main content

Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and Shiga toxin-producing Escherichia coli in asymptomatic nursery children in Lower Saxony (Germany), 2014

  • M. HARRIES (a1) (a2) (a3), J. DREESMAN (a4), S. RETTENBACHER-RIEFLER (a5) and E. MERTENS (a6)

Children may be at higher risk for carriage of antimicrobial-resistant bacteria because of higher usage of antimicrobials. They also have higher rates of Shiga toxin-producing Escherichia coli (STEC) infections than other population groups. Some infections, particularly in children, are asymptomatic, but still lead to the excretion of large numbers of bacteria and viruses that may cause clinical disease in other individuals. That is one reason why, in Lower Saxony as in other German federal states – asymptomatic carriers of STEC are excluded from nurseries and schools until three consecutive stool samples test negative in order to prevent secondary cases. The prevalence of children who are asymptomatic STEC carriers is unknown. But if it is high, this measure would have substantial socioeconomic effects on families. Infections with extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E) are an increasing problem for public health, especially for hospitals. However, there are no reliable estimates of the prevalence of asymptomatic ESBL-E carriers in Lower Saxony, as there is no mandatory requirement to report these carriers. In order to discuss the exclusion policies for children attending nurseries and ascertain a baseline of ESBL-E carriers, we conducted a cross-sectional study. The aim was to determine the prevalence of ESBL-E and STEC and identify risk factors for carriage in nursery children without diarrhoea (asymptomatic) aged 0–6 years in four selected districts in Northern Germany. During April–September 2014, we collected stool specimens with the support of voluntarily participating nurseries. We tested for STEC by PCR and for ESBL-E on chromogenic agar. Questionnaires answered by parents contained data on eating and drinking habits, outdoor activities, prior antibiotic treatment and animal contact for each participating child. We compared the epidemiological characteristics of ESBL-E carriers vs. non-carriers by using univariable analysis (P value, odds ratio and 95% confidence interval). We could not perform a statistical analysis for STEC carriers due to the low numbers of positive STEC specimens. Of 224 asymptomatic nursery children, we found a prevalence of 2·3% for ESBL-E carriage and 0·5% for STEC carriage. Asymptomatic ESBL-E carriers were more likely to have consumed raw milk, have had contact with pet rodents, or to have taken antibiotics during the preceding 6 months. We also found a high proportion of raw milk consumption (11%). We suggest that the low STEC prevalence in asymptomatic children supports the current practice of excluding STEC carriers from nurseries. The association between ESBL-E carriage and raw milk consumption and contact with pet rodents needs further investigation.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and Shiga toxin-producing Escherichia coli in asymptomatic nursery children in Lower Saxony (Germany), 2014
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and Shiga toxin-producing Escherichia coli in asymptomatic nursery children in Lower Saxony (Germany), 2014
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae and Shiga toxin-producing Escherichia coli in asymptomatic nursery children in Lower Saxony (Germany), 2014
      Available formats
Corresponding author
*Author for correspondence: Dr M. Harries, Governmental Institute of Public Health of Lower Saxony, Roesebeckstr. 4–6, D-30449 Hannover, Germany. (Email:
Hide All
1. O'Brien, AD, et al. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli . Journal of Infectious Diseases 1982; 146: 763769.
2. Pitout, JDD, Laupland, KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infectious Diseases 2008; 8: 159166.
3. Bundesgesetzblatt. Infectious disease control law in Germany 33 (Teil I-G5702): 1045–77 [in German] (
4. Frank, C, et al. Cattle density and Shiga toxin-producing Escherichia coli infection in Germany: increased risk for most but not all serogroups. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.) 2008; 8: 635643.
5. Buchholz, U, et al. German outbreak of Escherichia coli O104: H4 associated with sprouts. New England Journal of Medicine 2011; 365: 17631770.
6. Wahl, E, et al. Investigation of an Escherichia coli O145 outbreak in a child day-care centre – extensive sampling and characterization of eae- and stx1-positive E. coli yields epidemiological and socioeconomic insight. BMC Infectious Diseases 2011; 11: 238.
7. Dabke, G, et al. Duration of shedding of verocytotoxin-producing Escherichia coli in children and risk of transmission in childcare facilities in England. Epidemiology and Infection 2014; 142: 327334.
8. Kader, AA, Kumar, A, Kamath, KA. Fecal carriage of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in patients and asymptomatic healthy individuals. Infection Control and Hospital Epidemiology 2007; 28: 11141146.
9. Valenza, G, et al. Extended-spectrum-β-lactamase-producing Escherichia coli as intestinal colonizers in the German community. Antimicrobial Agents and Chemotherapy 2014; 58: 12281230.
10. Geser, N, et al. Molecular identification of extended-spectrum-β-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrobial Agents and Chemotherapy 2012; 56: 16091612.
11. Luvsansharav, U, et al. Prevalence of fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae among healthy adult people in Japan. Journal of Infection and Chemotherapy 2011; 17: 722725.
12. Livermore, DM, Woodford, N. The β-lactamase threat in Enterobacteriaceae, Pseudomonas and Acinetobacter . Trends in Microbiology 2006; 14: 413420.
13. Schechner, V, et al. Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clinical Microbiology Reviews 2013; 26: 289307.
14. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Paul-Ehrlich-Gesellschaft für Chemotherapie e.V., James D. Report on antibiotic consumption and the extent of resistance against antimicrobials in human and veterinary medicine, Germany, 2014 [in German].
15. Coque, TM, Baquero, F, Canton, R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Eurosurveillance 2008; 13: 19044.
16. Haller, S, et al. What caused the outbreak of ESBL-producing Klebsiella pneumoniae in a neonatal intensive care unit, Germany 2009 to 2012? Reconstructing transmission with epidemiological analysis and whole-genome sequencing. BMJ Open 2015; 5: e007397.
17. Thünen Institut. German maps of agricultural use (beef, veal and agricultural area), 2010 [in German] (
18. Ziehm, D, et al. Risk factors associated with sporadic salmonellosis in children: a case-control study in Lower Saxony, Germany (2008–2011). Epidemiology and Infection 2015; 143: 687694.
19. Reischl, U, et al. Real-time fluorescence PCR assays for detection and characterization of Shiga toxin, intimin, and enterohemolysin genes from Shiga toxin-producing Escherichia coli . Journal of Clinical Microbiology 2002; 40: 25552565.
20. Vogelsang, EPM. Environmental studies of asymptomatic kindergarten children as carriers of enterohemorrhagic Escherichia coli (EHEC) in the Ammerland district (Germany). Das Gesundheitswesen 1999; 61: 3844.
21. Dreesman, J, Röttgers, HR, Mellmann, APM. STEC outbreak with 59 cases after raw milk consumption in a summer camp [in German]. Das Gesundheitswesen 2007; 69: 1618.
22. Niedersächsisches Landesgesundheitsamt (NLGA). Screening of STEC in farmers in Lower Saxony 2012, unpublished raw data, 2012.
23. MacDonald, E, et al. Implications of screening and childcare exclusion policies for children with Shiga-toxin producing Escherichia coli infections: lessons learned from an outbreak in a daycare centre, Norway, 2012. BMC Infectious Diseases 2014; 14: 673.
24. Snedeker, KG, et al. Primary and secondary cases in Escherichia coli O157 outbreaks: a statistical analysis. BMC Infectious Diseases 2009; 9: 144.
25. Al-Jader, L, et al. Outbreak of Escherichia coli O157 in a nursery: lessons for prevention. Archives of Disease in Childhood 1999; 81: 6063.
26. Allaby, MA, Mayon-White, R. Escherichia coli O 157: outbreak in a day nursery. Communicable Disease Report. CDR Review 1995; 5: R46.
27. Abu-Sin, M, et al. Carrier prevalence, secondary household transmission, and long-term shedding in 2 districts during the Escherichia coli O104: H4 outbreak in Germany, 2011. Journal of Infectious Diseases 2013; 207: 432438.
28. Norwegian Institute of Public Health. Infection Control Book [in Norwegian], 2009.
29. Kaarme, J, et al. Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in healthy Swedish preschool children. Acta Paediatrica 2013; 102: 655660.
30. Guimaraes, B, et al. Genetic detection of extended-spectrum beta-lactamase-containing Escherichia coli isolates and vancomycin-resistant enterococci in fecal samples of healthy children. Microbial Drug Resistance (Larchmont, N.Y.) 2009; 15: 211216.
31. Birgy, A, et al. Community faecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in french children. BioMed Central 2012; 12: 315.
32. Meyer, E, et al. Pet animals and foreign travel are risk factors for colonisation with extended-spectrum β-lactamase-producing Escherichia coli . Infection 2012; 40: 685687.
33. Tham, J, et al. Risk factors for infections with extended-spectrum beta-lactamase-producing Escherichia coli in a county of Southern Sweden. Infection and Drug Resistance 2013; 6: 9397.
34. Valentin, L, et al. Subgrouping of ESBL-producing Escherichia coli from animal and human sources: an approach to quantify the distribution of ESBL types between different reservoirs. International Journal of Medical Microbiology 2014; 304: 805816.
35. Eller, C, et al. Extended-spectrum beta-lactamase (ESBL) in Escherichia coli in hospitals and outpatient sectors and general population [in German]. Abstract book, p. 10. German Medical Science GMS Publishing House, 2013.
36. Geser, N, Stephan, R, Hächler, H. Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Veterinary Research 2012; 8: 21.
37. European Centre for Disease Prevention and Control (ECDC). Surveillance Report: Antimicrobial resistance surveillance in Europe 2013 ( Accessed 18 August 2015.
38. Robert Koch-Institut (RKI). Antimicrobial resistance surveillance in Germany [in German] ( Accessed 19 August 2015.
39. Niedersächsisches Landesgesundheitsamt (NLGA). ARMIN. Antimicrobial resistance monitoring in Lower Saxony [in German] ( Accessed 19 August 2015.
40. Headrick, M, et al. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. American Journal of Public Health 1998; 88: 12191221.
41. Skočková, A, et al. Antimicrobial-resistant and extended-spectrum β-lactamase-producing Escherichia coli in raw cow's milk. Journal of Food Protection 2015; 78: 7277.
42. Rasheed, MU, et al. Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Revista do Instituto de Medicina Tropical de São Paulo 2014; 56: 341346.
43. Ewers, C, et al. Emergence of human pandemic O25: H4-ST131 CTX-M-15 extended-spectrum-lactamase-producing Escherichia coli among companion animals. Journal of Antimicrobial Chemotherapy 2010; 65: 651660.
44. Schmid, A, et al. Prevalence of extended-spectrum β-lactamase-producing Escherichia coli on Bavarian dairy and beef cattle farms. Applied and Environmental Microbiology 2013; 79: 30273032.
45. Guenther, S, et al. Is fecal carriage of extended-spectrum-β-lactamase-producing Escherichia coli in urban rats a risk for public health? Antimicrobial Agents and Chemotherapy 2013; 57: 24242425.
46. Ho, PL, et al. Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to ‘critically important’ antibiotics among food animals in Hong Kong, 2008–10. Journal of Antimicrobial Chemotherapy 2011; 66: 765768.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Epidemiology & Infection
  • ISSN: -
  • EISSN: 1469-4409
  • URL: /core/journals/epidemiology-and-infection
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed