Please cite this article in press as: Belmar Campos, C., et al., Prevalence and genotypes of extended spectrum beta-lactamases
in Enterobacteriaceae isolated from human stool and chicken meat in Hamburg, Germany. Int. J. Med. Microbiol. (2014),
http://dx.doi.org/10.1016/j.ijmm.2014.04.012
ARTICLE IN PRESS
G Model
IJMM-50820; No. of Pages 7
International Journal of Medical Microbiology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
International Journal of Medical Microbiology
j ourna l h o mepage: www.elsevier.com/locate/ijmm
Prevalence and genotypes of extended spectrum beta-lactamases in
Enterobacteriaceae isolated from human stool and chicken meat in
Hamburg, Germany
Cristina Belmar Campos
a,∗
, Ines Fenner
b
, Nicole Wiese
b
, Carmen Lensing
b
,
Martin Christner
a
, Holger Rohde
a
, Martin Aepfelbacher
a
, Thomas Fenner
b
,
Moritz Hentschke
a
a
Institute of Medical Microbiology, Virology and Hygiene, University Medical Centre Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany
b
Fen-Lab GmbH, Bergstrasse 14, 20095 Hamburg, Germany
a r t i c l e i n f o
Article history:
Received 24 September 2013
Received in revised form 22 April 2014
Accepted 27 April 2014
Keywords:
ESBL
Poultry
Emergency department
Sequence type
a b s t r a c t
Chicken meat has been proposed to constitute a source for extended spectrum beta-lactamase
(ESBL)-carrying Enterobacteriaceae that colonize and infect humans. In this study the prevalence of ESBL-
producing Enterobacteriaceae in stool samples from ambulatory patients who presented in the emergency
department of the University Medical Centre Hamburg-Eppendorf with gastrointestinal complains and
in chicken meat samples from the Hamburg region were analysed and compared with respect to ESBL-
genotypes, sequence types and antibiotic resistance profiles. Twenty-nine (4.1%) of 707 stool samples
and 72 (60%) of 120 chicken meat samples were positive for ESBL-producing Enterobacteriaceae. The dis-
tribution of ESBL genes in the stool vs. chicken meat isolates (given as % of total isolates from stool vs.
chicken meat) was as follows: CTX-M-15 (38% vs. 0%), CTX-M-14 (17% vs. 6%), CTX-M-1 (17% vs. 69%),
SHV-12 (3% vs. 18%) and TEM-52 (3% each). Comparison of ESBL- and multilocus sequence type revealed
no correlation between isolates of human and chicken. Furthermore, ESBL-producing E. coli from stool
samples were significantly more resistant to fluoroquinolones, aminoglycosides and/or trimethoprim-
sulfamethoxazole than chicken isolates. The differences in ESBL-genotypes, sequence types and antibiotic
resistance patterns indicate that in our clinical setting chicken meat is not a major contributor to human
colonization with ESBL-carrying Enterobacteriaceae.
© 2014 Elsevier GmbH. All rights reserved.
Introduction
Prevalence of and infections due to ESBL-positive Enterobacteri-
aceae are rapidly increasing in Europe (Coque et al., 2008; de Kraker
et al., 2011) and are associated with an increased mortality, longer
hospital stays and increased costs (de Kraker et al., 2011; Gastmeier
et al., 2012). Resistance to third generation cephalosporines in
Escherichia coli and Klebsiella pneumoniae is mainly mediated by
plasmid-encoded extended spectrum beta-lactamases (Bradford,
2001). They include enzymes from the CTX-M-group, the TEM-
group and the SHV-group (Canton et al., 2008; Paterson and
Bonomo, 2005). The epidemiology of ESBL genes has changed dur-
ing the last decade particularly in Europe (Livermore et al., 2007).
In former years ESBL genes mainly spread in K. pneumoniae in the
hospital environment and were of the classical TEM- and SHV-type,
∗
Corresponding author. Tel.: +49 40 7410 59728; fax: +49 40 7410 53250.
E-mail address: c.belmar-campos@uke.de (C. Belmar Campos).
which are allelic variants of TEM-1, TEM-2 and SHV-1 with an
increased activity towards extended spectrum cephalosporines
(Bradford, 2001). Nowadays ESBL genes are much more frequently
found in E. coli the majority of which belongs to the CTX-M- group
(Livermore et al., 2007; Rossolini et al., 2008; Canton et al., 2012).
ESBL-positive E. coli are currently believed to be often acquired
outside the hospital (Pitout and Laupland, 2008) while nosocomial
transmission seems less efficient (Tschudin-Sutter et al., 2012).
Therefore, ESBL infections in the hospital are mainly considered
as an imported problem and standard hygiene precautions may be
insufficient to stop the increase in ESBL prevalence.
A number of studies have analysed carriage rates of ESBL-
expressing Enterobacteriaceae in non-hospitalized humans in
different European countries (Cekanova et al., 2009; Geser et al.,
2012; Hammerum et al., 2011; Paniagua et al., 2010; Reuland
et al., 2013; Stromdahl et al., 2011; Valverde et al., 2004) and
found prevalence rates from 1.2% in the Czech Republic (Cekanova
et al., 2009) to 10.1% in the Netherlands (Reuland et al., 2013). The
source of human colonization is currently unknown. High ESBL
http://dx.doi.org/10.1016/j.ijmm.2014.04.012
1438-4221/© 2014 Elsevier GmbH. All rights reserved.