Clonal Structure, Extended-Spectrum β-Lactamases, and Acquired AmpC-Type Cephalosporinases of Escherichia coli Populations Colonizing Patients in Rehabilitation Centers in Four Countries

ABSTRACT The prospective project MOSAR was conducted in five rehabilitation units: the Berck Maritime Hôpital (Berck, France), Fondazione Santa Lucia (Rome, Italy), Guttmann Institute (GI; Barcelona, Spain), and Loewenstein Hospital and Tel-Aviv Souraski Medical Center (TA) (Tel-Aviv, Israel). Patients were screened for carriage of Enterobacteriaceae resistant to expanded-spectrum cephalosporins (ESCs) from admission until discharge. The aim of this study was to characterize the clonal structure, extended-spectrum β-lactamases (ESBLs), and acquired AmpC-like cephalosporinases in the Escherichia coli populations collected. A total of 376 isolates were randomly selected. The overall number of sequence types (STs) was 76, including 7 STs that grouped at least 10 isolates from at least three centers each, namely, STs 10, 38, 69, 131, 405, 410, and 648. These clones comprised 65.2% of all isolates, and ST131 alone comprised 41.2%. Of 54 STs observed only in one center, some STs played a locally significant role, like ST156 and ST393 in GI or ST372 and ST398 in TA. Among 16 new STs, five arose from evolution within the ST10 and ST131 clonal complexes. ESBLs and AmpCs accounted for 94.7% and 5.6% of the ESC-hydrolyzing β-lactamases, respectively, being dominated by the CTX-M-like enzymes (79.9%), followed by the SHV (13.5%) and CMY-2 (5.3%) types. CTX-M-15 was the most prevalent β-lactamase overall (40.6%); other ubiquitous enzymes were CTX-M-14 and CMY-2. Almost none of the common clones correlated strictly with one β-lactamase; although 58.7% of ST131 isolates produced CTX-M-15, the clone also expressed nine other enzymes. A number of clone variants with specific pulsed-field gel electrophoresis and ESBL types were spread in some locales, potentially representing newly emerging E. coli epidemic strains.

[1]  H. Goossens,et al.  Transmission dynamics of ESBL-producing Escherichia coli clones in rehabilitation wards at a tertiary care centre. , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[2]  H. Goossens,et al.  Characterization of Two New CTX-M-25-Group Extended-Spectrum β-Lactamase Variants Identified in Escherichia coli Isolates from Israel , 2012, PloS one.

[3]  N. Woodford,et al.  Characterization of Enterobacteriaceae producing OXA-48-like carbapenemases in the UK. , 2012, The Journal of antimicrobial chemotherapy.

[4]  A. Boudabous,et al.  Prevalence and characterisation of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli isolates in healthy volunteers in Tunisia , 2012, European Journal of Clinical Microbiology & Infectious Diseases.

[5]  I. Luzzi,et al.  Escherichia coli of human and avian origin: detection of clonal groups associated with fluoroquinolone and multidrug resistance in Italy. , 2012, The Journal of antimicrobial chemotherapy.

[6]  A. Robicsek,et al.  Comparison of Escherichia coli ST131 Pulsotypes, by Epidemiologic Traits, 1967–2009 , 2012, Emerging infectious diseases.

[7]  G. Peirano,et al.  The presence of genes encoding for different virulence factors in clonally related Escherichia coli that produce CTX-Ms. , 2012, Diagnostic microbiology and infectious disease.

[8]  J. Quinn,et al.  Molecular Epidemiological Analysis of Escherichia coli Sequence Type ST131 (O25:H4) and blaCTX-M-15 among Extended-Spectrum-β-Lactamase-Producing E. coli from the United States, 2000 to 2009 , 2012, Antimicrobial Agents and Chemotherapy.

[9]  J. Cheesbrough,et al.  Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from Northwest England. , 2012, The Journal of antimicrobial chemotherapy.

[10]  G. Peirano,et al.  Molecular Epidemiology over an 11-Year Period (2000 to 2010) of Extended-Spectrum β-Lactamase-Producing Escherichia coli Causing Bacteremia in a Centralized Canadian Region , 2011, Journal of Clinical Microbiology.

[11]  J. Blanco,et al.  National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. , 2011, The Journal of antimicrobial chemotherapy.

[12]  N. Woodford,et al.  Phylogenetic diversity of Escherichia coli strains producing NDM-type carbapenemases. , 2011, The Journal of antimicrobial chemotherapy.

[13]  N. Woodford,et al.  Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. , 2011, FEMS microbiology reviews.

[14]  P. Nordmann,et al.  When Carbapenem-Hydrolyzing β-Lactamase KPC Meets Escherichia coli ST131 in France , 2011, Antimicrobial Agents and Chemotherapy.

[15]  G. Peirano,et al.  Molecular characteristics of extended-spectrum β-lactamase-producing Escherichia coli from Rio de Janeiro, Brazil. , 2011, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[16]  G. Peirano,et al.  Clinical and Molecular Characteristics of Extended-Spectrum- β-Lactamase-Producing Escherichia coli Causing Bacteremia in the Rotterdam Area, Netherlands , 2011, Antimicrobial Agents and Chemotherapy.

[17]  J. Klena,et al.  CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. , 2011, Microbial drug resistance.

[18]  J. Blanco,et al.  Spread of Escherichia coli O25b:H4-B2-ST131 producing CTX-M-15 and SHV-12 with high virulence gene content in Barcelona (Spain). , 2011, The Journal of antimicrobial chemotherapy.

[19]  J. Hrabák,et al.  DHA-1-producing Klebsiella pneumoniae in a teaching hospital in the Czech Republic. , 2010, Microbial drug resistance.

[20]  A. Carattoli,et al.  Ciprofloxacin-resistant, CTX-M-15-producing Escherichia coli ST131 clone in extraintestinal infections in Italy. , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[21]  J. Campos,et al.  Extended-spectrum β-lactamase producing Escherichia coli: changing epidemiology and clinical impact , 2010 .

[22]  R. Moreau,et al.  Genetic Diversity and Virulence Profiles of Escherichia coli Isolates Causing Spontaneous Bacterial Peritonitis and Bacteremia in Patients with Cirrhosis , 2010, Journal of Clinical Microbiology.

[23]  Richard J. Reid-Smith,et al.  Food Reservoir for Escherichia coli Causing Urinary Tract Infections , 2010, Emerging infectious diseases.

[24]  E. Denamur,et al.  Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. , 2009, The Journal of antimicrobial chemotherapy.

[25]  J. Campos,et al.  Extended-spectrum beta-lactamase-producing Escherichia coli in Spain belong to a large variety of multilocus sequence typing types, including ST10 complex/A, ST23 complex/A and ST131/B2. , 2009, International journal of antimicrobial agents.

[26]  P. Barrow,et al.  Enterobacteriaceae , 2008, Poultry Diseases.

[27]  M. Kuskowski,et al.  Epidemic Clonal Groups of Escherichia coli as a Cause of Antimicrobial-Resistant Urinary Tract Infections in Canada, 2002 to 2004 , 2009, Antimicrobial Agents and Chemotherapy.

[28]  Alessandra Carattoli,et al.  Resistance Plasmid Families in Enterobacteriaceae , 2009, Antimicrobial Agents and Chemotherapy.

[29]  George A. Jacoby,et al.  AmpC β-Lactamases , 2009, Clinical Microbiology Reviews.

[30]  M. Kaufmann,et al.  UK epidemic Escherichia coli strains A-E, with CTX-M-15 beta-lactamase, all belong to the international O25:H4-ST131 clone. , 2008, The Journal of antimicrobial chemotherapy.

[31]  Y. Arakawa,et al.  Change in the prevalence of extended-spectrum-beta-lactamase-producing Escherichia coli in Japan by clonal spread. , 2008, The Journal of antimicrobial chemotherapy.

[32]  L. Guize,et al.  Absence of CTX-M Enzymes but High Prevalence of Clones, Including Clone ST131, among Fecal Escherichia coli Isolates from Healthy Subjects Living in the Area of Paris, France , 2008, Journal of Clinical Microbiology.

[33]  Y. Carmeli,et al.  Dissemination of the CTX-M-25 family beta-lactamases among Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae and identification of the novel enzyme CTX-M-41 in Proteus mirabilis in Israel. , 2008, The Journal of antimicrobial chemotherapy.

[34]  A. Marchese,et al.  European Emergence of Ciprofloxacin-Resistant Escherichia coli Clonal Groups O25:H4-ST 131 and O15:K52:H1 Causing Community-Acquired Uncomplicated Cystitis , 2008, Journal of Clinical Microbiology.

[35]  E. Sadowy,et al.  Molecular Survey of β-Lactamases Conferring Resistance to Newer β-Lactams in Enterobacteriaceae Isolates from Polish Hospitals , 2008, Antimicrobial Agents and Chemotherapy.

[36]  K. Laupland,et al.  Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern , 2008 .

[37]  F. Baquero,et al.  Dissemination of Clonally Related Escherichia coli Strains Expressing Extended-Spectrum β-Lactamase CTX-M-15 , 2008, Emerging infectious diseases.

[38]  J. Blanco,et al.  Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. , 2007, The Journal of antimicrobial chemotherapy.

[39]  N. Woodford,et al.  CTX-M: changing the face of ESBLs in Europe. , 2006, The Journal of antimicrobial chemotherapy.

[40]  G. Rossolini,et al.  CTX-M-Type Extended-Spectrum β-Lactamases in Italy: Molecular Epidemiology of an Emerging Countrywide Problem , 2006, Antimicrobial Agents and Chemotherapy.

[41]  Daniel Falush,et al.  Sex and virulence in Escherichia coli: an evolutionary perspective , 2006, Molecular microbiology.

[42]  D. Livermore,et al.  CTX-M: changing the face of ESBLs in the UK. , 2005, The Journal of antimicrobial chemotherapy.

[43]  E. Sadowy,et al.  Four Variants of the Citrobacter freundii AmpC-Type Cephalosporinases, Including Novel Enzymes CMY-14 and CMY-15, in a Proteus mirabilis Clone Widespread in Poland , 2004, Antimicrobial Agents and Chemotherapy.

[44]  N. Hanson,et al.  Detection of Plasmid-Mediated AmpC β-Lactamase Genes in Clinical Isolates by Using Multiplex PCR , 2002, Journal of Clinical Microbiology.

[45]  Gregor Tanner,et al.  Determining Confidence Intervals When Measuring Genetic Diversity and the Discriminatory Abilities of Typing Methods for Microorganisms , 2001, Journal of Clinical Microbiology.

[46]  P. Bradford Extended-Spectrum β-Lactamases in the 21st Century: Characterization, Epidemiology, and Detection of This Important Resistance Threat , 2001, Clinical Microbiology Reviews.

[47]  R. Bonnet,et al.  A 1998 Survey of Extended-Spectrum β-Lactamases in Enterobacteriaceae in France , 2000, Antimicrobial Agents and Chemotherapy.

[48]  O. Clermont,et al.  Rapid and Simple Determination of theEscherichia coli Phylogenetic Group , 2000, Applied and Environmental Microbiology.

[49]  D. F. Sahm,et al.  AmpC beta-lactamases. , 1998 .

[50]  D H Persing,et al.  Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing , 1995, Journal of clinical microbiology.

[51]  M. Struelens,et al.  Pseudomonas aeruginosa and Enterobacteriaceae bacteremia after biliary endoscopy: an outbreak investigation using DNA macrorestriction analysis. , 1993, The American journal of medicine.

[52]  A. Bauernfeind,et al.  A new plasmidic cefotaximase in a clinical isolate of Escherichia coli , 1990, Infection.

[53]  D. Paterson,et al.  Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. , 2011, The Journal of antimicrobial chemotherapy.

[54]  V. Jarlier,et al.  Phenotypic detection of extended-spectrum beta-lactamase production in Enterobacteriaceae: review and bench guide. , 2008, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[55]  G. Rossolini,et al.  The spread of CTX-M-type extended-spectrum β-lactamases , 2008 .

[56]  N. Woodford,et al.  Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum (beta)-lactamases. , 2006, The Journal of antimicrobial chemotherapy.