CTX-M ESBL-producing Enterobacteriaceae: estimated prevalence in adults in England in 2014

Abstract Background ESBL-producing Enterobacteriaceae (ESBLPE) are increasing in prevalence worldwide and are more difficult to treat than non-ESBLPE. Their prevalence in the UK general population is unknown, as the only previous UK ESBLPE faecal colonization study involved patients with diarrhoea. Objectives To estimate the prevalence of CTX-M ESBLPE faecal colonization in the general adult population of England in 2014, and investigate risk factors. Methods A stratified random sample of 58 337 registered patients from 16 general practices within four areas of England were invited to participate by returning faeces specimens and self-completed questionnaires. Specimens were tested for ESBLPE and carbapenemase-producing Enterobacteriaceae (CPE). Results 2430 individuals participated (4% of those invited). The estimated prevalence of colonization with CTX-M ESBLPE in England was 7.3% (95% CI 5.6%–9.4%) (Shropshire 774 participants, 4.9% colonization; Southampton City 740 participants, 9.2%; Newham 612 participants, 12.7%; Heart of Birmingham 234 individuals, 16.0%) and was particularly high in: those born in Afghanistan (10 participants, 60.0% colonization, 95% CI 29.7%–84.2%); those born on the Indian subcontinent (India, Pakistan, Bangladesh or Sri Lanka) (259 participants, 25.0% colonization, 95% CI 18.5%–32.9%); travellers to South Asia (India, Pakistan, Bangladesh, Sri Lanka or Nepal) in the last year (140 participants, 38.5% colonization, 95% CI 27.8%–50.5%); and healthcare domestics (8 participants, unweighted 37.5% colonization, 95% CI 8.5%–75.5%). Risk factors identified included: being born in the Indian subcontinent (aOR 5.4, 95% CI 3.0–9.7); travel to South Asia (aOR 2.9, 95% CI 1.8–4.8) or to Africa, China, South or Central America, South East or Pacific Asia or Afghanistan (aOR 2.6, 95% CI 1.7–4.1) in the last year; and working as a healthcare domestic (aOR 6.2, 95% CI 1.3–31). None of the 48 participants who took co-amoxiclav in the last year was colonized with CTX-M ESBLPE. blaCTX-M-15 accounted for 66% of CTX-M ESBLPE positives. 0.1% (two participants) were colonized with CPE. Conclusions CTX-M ESBLPE are established in the general population in England and prevalence is particularly high in people from certain countries of birth or with recent travel. We recommend that these findings be taken into account in guidance on the empirical management of patients presenting with a likely Enterobacteriaceae infection.

[1]  Sepsis: recognition, diagnosis and early management , 2018, BJU international.

[2]  C. Mcnulty,et al.  Treatment of infections caused by multidrug-resistant Gram-negative bacteria: report of the British Society for Antimicrobial Chemotherapy/Healthcare Infection Society/British Infection Association Joint Working Party† , 2018, The Journal of antimicrobial chemotherapy.

[3]  P. Hawkey,et al.  Global epidemiology of CTX-M &bgr;-lactamases: temporal and geographical shifts in genotype , 2017, The Journal of antimicrobial chemotherapy.

[4]  S. Schwarz,et al.  Extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolates collected from diseased food-producing animals in the GERM-Vet monitoring program 2008-2014. , 2017, Veterinary microbiology.

[5]  D. Heederik,et al.  Extended-spectrum β-lactamase- and pAmpC-producing Enterobacteriaceae among the general population in a livestock-dense area. , 2017, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[6]  N. Woodford,et al.  Characterization of carbapenemase-producing Enterobacteriaceae in the West Midlands region of England: 2007–14 , 2017, The Journal of antimicrobial chemotherapy.

[7]  E. Vincent Managing common infections: guidance for primary care , 2016 .

[8]  P. V. van Genderen,et al.  Prolonged carriage and potential onward transmission of carbapenemase-producing Enterobacteriaceae in Dutch travelers. , 2016, Future microbiology.

[9]  S. Karanika,et al.  Fecal Colonization With Extended-spectrum Beta-lactamase-Producing Enterobacteriaceae and Risk Factors Among Healthy Individuals: A Systematic Review and Metaanalysis. , 2016, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[10]  M. Woodward,et al.  Genetic & virulence profiling of ESBL-positive E. coli from nosocomial & veterinary sources. , 2016, Veterinary microbiology.

[11]  L. Wieler,et al.  High carriage rate of ESBL-producing Enterobacteriaceae at presentation and follow-up among travellers with gastrointestinal complaints returning from India and Southeast Asia. , 2016, Journal of travel medicine.

[12]  P. Savelkoul,et al.  Prevalence and risk factors for carriage of ESBL-producing Enterobacteriaceae in Amsterdam , 2016, The Journal of antimicrobial chemotherapy.

[13]  R. Hein,et al.  Use of an Enrichment Broth Improves Detection of Extended-Spectrum-Beta-Lactamase-Producing Enterobacteriaceae in Clinical Stool Samples , 2015, Journal of Clinical Microbiology.

[14]  L. Epelboin,et al.  High Rate of Multidrug-Resistant Gram-Negative Bacilli Carriage and Infection in Hospitalized Returning Travelers: A Cross-Sectional Cohort Study. , 2015, Journal of travel medicine.

[15]  M. Esposito‐Farèse,et al.  High Rate of Acquisition but Short Duration of Carriage of Multidrug-Resistant Enterobacteriaceae After Travel to the Tropics. , 2015, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[16]  P. Collignon,et al.  Long-term persistence of multidrug-resistant Enterobacteriaceae after travel. , 2015, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[17]  R. Saranathan,et al.  Simultaneous gut colonisation and infection by ESBL-producing Escherichia coli in hospitalised patients. , 2015, The Australasian medical journal.

[18]  N. Woodford,et al.  Surveillance of antibiotic susceptibility of urinary tract pathogens for a population of 5.6 million over 4 years. , 2015, The Journal of antimicrobial chemotherapy.

[19]  P. Hawkey,et al.  Multidrug-resistant Gram-negative bacteria: a product of globalization. , 2015, The Journal of hospital infection.

[20]  J. Ollgren,et al.  Antimicrobials Increase Travelers' Risk of Colonization by Extended-Spectrum Betalactamase-Producing Enterobacteriaceae , 2015, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[21]  G. Feierl,et al.  Isolation and characterization of multidrug-resistant bacteria from minced meat in Austria. , 2014, Food microbiology.

[22]  A. V. van Hoek,et al.  Extended-spectrum and AmpC β-lactamase-producing Escherichia coli in broilers and people living and/or working on broiler farms: prevalence, risk factors and molecular characteristics. , 2014, The Journal of antimicrobial chemotherapy.

[23]  M. Battegay,et al.  High colonization rates of extended-spectrum β-lactamase (ESBL)-producing Escherichia coliin Swiss Travellers to South Asia– a prospective observational multicentre cohort study looking at epidemiology, microbiology and risk factors , 2014, BMC Infectious Diseases.

[24]  N. Ahmed,et al.  Genotypic and Phenotypic Profiles of Escherichia coli Isolates Belonging to Clinical Sequence Type 131 (ST131), Clinical Non-ST131, and Fecal Non-ST131 Lineages from India , 2014, Antimicrobial Agents and Chemotherapy.

[25]  D. Livermore,et al.  Homogeneity of antimicrobial policy, yet heterogeneity of antimicrobial resistance: antimicrobial non-susceptibility among 108 717 clinical isolates from primary, secondary and tertiary care patients in London , 2014, The Journal of antimicrobial chemotherapy.

[26]  P. Woerther,et al.  Trends in Human Fecal Carriage of Extended-Spectrum β-Lactamases in the Community: Toward the Globalization of CTX-M , 2013, Clinical Microbiology Reviews.

[27]  M. Wilcox,et al.  Surveillance of antibiotic susceptibility of Enterobacteriaceae isolated from urine samples collected from community patients in a large metropolitan area, 2010–2012 , 2013, Epidemiology and Infection.

[28]  J. Verhaegen,et al.  Evaluation of 3 different agar media for rapid detection of extended-spectrum β-lactamase-producing Enterobacteriaceae from surveillance samples. , 2013, Diagnostic microbiology and infectious disease.

[29]  K. Harris,et al.  Risk factors associated with extended spectrum beta-lactamase Escherichia coli (CTX-M) on dairy farms in North West England and North Wales. , 2012, Preventive veterinary medicine.

[30]  M. Kalin,et al.  Prevalence of antibiotic-resistant bacteria in residents of nursing homes in a Swedish municipality: Healthcare staff knowledge of and adherence to principles of basic infection prevention , 2012, Scandinavian journal of infectious diseases.

[31]  M. Fielder,et al.  Detection and characterization of pCT-like plasmid vectors for blaCTX-M-14 in Escherichia coli isolates from humans, turkeys and cattle in England and Wales. , 2012, The Journal of antimicrobial chemotherapy.

[32]  P. Hawkey,et al.  High community faecal carriage rates of CTX-M ESBL-producing Escherichia coli in a specific population group in Birmingham, UK. , 2012, The Journal of antimicrobial chemotherapy.

[33]  F. Baquero,et al.  Fecal Carriage of Carbapenemase-Producing Enterobacteriaceae: a Hidden Reservoir in Hospitalized and Nonhospitalized Patients , 2012, Journal of Clinical Microbiology.

[34]  R. Cantón,et al.  CTX-M Enzymes: Origin and Diffusion , 2012, Front. Microbio..

[35]  K. Nye,et al.  Regional survey of CTX-M-type extended-spectrum β-lactamases among Enterobacteriaceae reveals marked heterogeneity in the distribution of the ST131 clone. , 2011, The Journal of antimicrobial chemotherapy.

[36]  M. Hayden,et al.  Direct Ertapenem Disk Screening Method for Identification of KPC-Producing Klebsiella pneumoniae and Escherichia coli in Surveillance Swab Specimens , 2010, Journal of Clinical Microbiology.

[37]  F. Baquero,et al.  Spread of blaCTX-M-14 Is Driven Mainly by IncK Plasmids Disseminated among Escherichia coli Phylogroups A, B1, and D in Spain , 2009, Antimicrobial Agents and Chemotherapy.

[38]  P. Hawkey,et al.  The changing epidemiology of resistance. , 2009, The Journal of antimicrobial chemotherapy.

[39]  J. Rodríguez-Baño,et al.  Faecal carriage of extended-spectrum beta-lactamase-producing Escherichia coli: prevalence, risk factors and molecular epidemiology. , 2008, The Journal of antimicrobial chemotherapy.

[40]  J. Morris,et al.  Patient-to-patient transmission is important in extended-spectrum beta-lactamase-producing Klebsiella pneumoniae acquisition. , 2007, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[41]  V. Ensor,et al.  Occurrence, prevalence and genetic environment of CTX-M beta-lactamases in Enterobacteriaceae from Indian hospitals. , 2006, The Journal of antimicrobial chemotherapy.

[42]  M. Cetron,et al.  Spectrum of disease and relation to place of exposure among ill returned travelers. , 2006, The New England journal of medicine.

[43]  V. Ensor,et al.  Rapid and simple detection of blaCTX-M genes by multiplex PCR assay. , 2005, Journal of medical microbiology.

[44]  J. Metlay,et al.  Test Characteristics of Perirectal and Rectal Swab Compared to Stool Sample for Detection of Fluoroquinolone-Resistant Escherichia coli in the Gastrointestinal Tract , 2005, Antimicrobial Agents and Chemotherapy.

[45]  R. Steffen,et al.  Travel epidemiology--a global perspective. , 2003, International journal of antimicrobial agents.

[46]  P. Silcocks,et al.  An assessment of the Nam Pehchan computer program for the identification of names of south Asian ethnic origin. , 1999, Journal of public health medicine.

[47]  P. V. van Genderen,et al.  Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. , 2017, The Lancet. Infectious diseases.

[48]  M. Wilcox,et al.  Escherichia coli bacteraemia: 2 years of prospective regional surveillance (2010-12). , 2014, The Journal of antimicrobial chemotherapy.

[49]  P. Savelkoul,et al.  High rates of antimicrobial drug resistance gene acquisition after international travel, The Netherlands. , 2014, Emerging infectious diseases.