Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 9/2016

01-09-2016 | Original Article

Emergence of co-production of plasmid-mediated AmpC beta-lactamase and ESBL in cefoxitin-resistant uropathogenic Escherichia coli

Authors: B. Ghosh, M. Mukherjee

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 9/2016

Login to get access

Abstract

Plasmid-mediated AmpC (pAmpC) and ESBL co-production was detected in Escherichia coli a major etiologic agent of urinary tract infection. Isolates resistant to cefoxitin by CLSI methodology were tested for pAmpC beta-lactamase using phenylboronic acid and ESBLs by combined disk diffusion method. pAmpC/ESBL genes were characterized by PCR and sequencing. Transconjugation experiments were done to study the transfer of pAmpC and ESBL production from clinical isolates as donor to E. coli J53 AziR as recipient. Incompatibility groups of transmissible plasmids were classified by PCR-based replicon typing (PBRT). Among 148 urine culture positive isolates, E. coli was reported in 39.86 % (59/148), with 93.22 % (55/59) of cefoxitin resistance. pAmpC production was detected in 25, with varied distribution of blaCMY-2 and blaDHA-1type genes alone (n = 13 and 7 respectively) or in combination (n = 5). ESBL co-production was observed in 88 % (22/25) of pAmpC producing isolates with predominance of blaTEM (n = 20). Twenty-three transconjugants showed transmission of pAmpC-and ESBL-resistant genes with co-carriage of blaCMY-2 and blaTEM (n = 15) in plasmids of IncF type (n = 9) being predominant, followed by IncI1 (n = 4) and IncH1 (n = 2) in combination. All clinical isolates were clonally diverse. Resistance against different beta-lactams in uropathogenic E. coli has been an emerging concern in resource- poor countries such as India. Knowledge on the occurrence of AmpC beta-lactamases and ESBL amongst this pathogen and its transmission dynamics may aid in hospital infection control.
Appendix
Available only for authorised users
Literature
1.
go back to reference Akram M, Shahid M, Khan AU (2007) Etiology and antibiotic resistance pattern of community-acquired urinary tract infection in JNMC Hospital Aligarh India. Ann Clin Microbiol Antimicrob 6:4–10CrossRefPubMedPubMedCentral Akram M, Shahid M, Khan AU (2007) Etiology and antibiotic resistance pattern of community-acquired urinary tract infection in JNMC Hospital Aligarh India. Ann Clin Microbiol Antimicrob 6:4–10CrossRefPubMedPubMedCentral
2.
go back to reference Nicolle LE (2007) Uncomplicated urinary tract infection in adults including uncomplicated pyelonephritis. Urol Clin N Am 35(1):1–12CrossRef Nicolle LE (2007) Uncomplicated urinary tract infection in adults including uncomplicated pyelonephritis. Urol Clin N Am 35(1):1–12CrossRef
3.
go back to reference Gales AC, Jones RN, Gordon KA et al (2000) Activity and spectrum of 22 antimicrobial agents tested against urinary tract pathogens in hospitalised patients in Latin America: report from the second year of the SENTRY Antimicrobial Surveillance Program (1998). J Antimicrob Chemother 45:295–303CrossRefPubMed Gales AC, Jones RN, Gordon KA et al (2000) Activity and spectrum of 22 antimicrobial agents tested against urinary tract pathogens in hospitalised patients in Latin America: report from the second year of the SENTRY Antimicrobial Surveillance Program (1998). J Antimicrob Chemother 45:295–303CrossRefPubMed
4.
go back to reference Gupta K, Sahm DF, Mayfield D et al (2001) Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in women: a nationwide analysis. Clin Infect Dis 33:89–94CrossRefPubMed Gupta K, Sahm DF, Mayfield D et al (2001) Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in women: a nationwide analysis. Clin Infect Dis 33:89–94CrossRefPubMed
5.
go back to reference Pérez-Pérez FJ, Hanson ND (2002) Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40(6):2153–2162CrossRefPubMedPubMedCentral Pérez-Pérez FJ, Hanson ND (2002) Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40(6):2153–2162CrossRefPubMedPubMedCentral
6.
go back to reference Mammeri H, Nazic H, Naas T et al (2004) AmpC β-Lactamase in an Escherichia coli Clinical isolate confers resistance to expanded-spectrum cephalosporins. Antimicrob Agents Chemother 48(10):4050–4053CrossRefPubMedPubMedCentral Mammeri H, Nazic H, Naas T et al (2004) AmpC β-Lactamase in an Escherichia coli Clinical isolate confers resistance to expanded-spectrum cephalosporins. Antimicrob Agents Chemother 48(10):4050–4053CrossRefPubMedPubMedCentral
7.
go back to reference Taneja N, Rao P, Arora J et al (2008) Occurrence of ESBL & Amp-C β-lactamases and susceptibility to newer antimicrobial agents in complicated UTI. Indian J Med Res 127:85–88PubMed Taneja N, Rao P, Arora J et al (2008) Occurrence of ESBL & Amp-C β-lactamases and susceptibility to newer antimicrobial agents in complicated UTI. Indian J Med Res 127:85–88PubMed
8.
go back to reference Manoharan A, Sugumar M, Kumar A et al (2012) Phenotypic and molecular characterization of AmpC βlactamases among Escherichia coli Klebsiella spp & Enterobacter spp from five Indian medical centers. Indian J Med Res 135:359–364PubMedPubMedCentral Manoharan A, Sugumar M, Kumar A et al (2012) Phenotypic and molecular characterization of AmpC βlactamases among Escherichia coli Klebsiella spp & Enterobacter spp from five Indian medical centers. Indian J Med Res 135:359–364PubMedPubMedCentral
9.
go back to reference Mohamudha PR, Harish BN, Parija SC (2012) Molecular description of plasmid-mediated AmpC β-lactamases among nosocomial isolates of Escherichia coli & Klebsiella pneumoniae from six different hospitals in India. Indian J Med Res 135:114–119CrossRefPubMedPubMedCentral Mohamudha PR, Harish BN, Parija SC (2012) Molecular description of plasmid-mediated AmpC β-lactamases among nosocomial isolates of Escherichia coli & Klebsiella pneumoniae from six different hospitals in India. Indian J Med Res 135:114–119CrossRefPubMedPubMedCentral
10.
go back to reference Chakraborty A, Adhikari P, Shenoy S et al (2014) Characterization of Plasmid mediated AmpC producing Escherechia coli clinical isolates from tertiary care hospital in South India. Indian J Pathol Microbiol 57(2):255–258CrossRefPubMed Chakraborty A, Adhikari P, Shenoy S et al (2014) Characterization of Plasmid mediated AmpC producing Escherechia coli clinical isolates from tertiary care hospital in South India. Indian J Pathol Microbiol 57(2):255–258CrossRefPubMed
11.
go back to reference Haenni M, Châtre P, Madec JY (2014) Emergence of Escherichiacoli producing extended-spectrum AmpCβ-lactamases(ESAC)in animals. Frontiers Microbiol 5(53):1–7 Haenni M, Châtre P, Madec JY (2014) Emergence of Escherichiacoli producing extended-spectrum AmpCβ-lactamases(ESAC)in animals. Frontiers Microbiol 5(53):1–7
13.
go back to reference Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300:371–379CrossRefPubMed Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300:371–379CrossRefPubMed
14.
go back to reference Swaminathan B, Barrett T, Hunter SB et al (2001) The molecular subtyping network for foodborne disease surveillance in the United States. Emerg Infect Dis 7:382–389CrossRefPubMedPubMedCentral Swaminathan B, Barrett T, Hunter SB et al (2001) The molecular subtyping network for foodborne disease surveillance in the United States. Emerg Infect Dis 7:382–389CrossRefPubMedPubMedCentral
15.
go back to reference Hanson ND (2003) AmpC β-lactamases: what do we need to know for the future? J Antimicrob Chemother 52:2–4CrossRefPubMed Hanson ND (2003) AmpC β-lactamases: what do we need to know for the future? J Antimicrob Chemother 52:2–4CrossRefPubMed
16.
go back to reference Papanicolaou GA, Medeiros AA, Jacoby GA (1990) Novel plasmid mediated β-lactamases(MIR-1) conferring resistance to oxyimino and α methoxy β-lactams in clinical isolates of Klebsiella pneumoniae. Antimicrob Agents Chemother 34:2200–2209CrossRefPubMedPubMedCentral Papanicolaou GA, Medeiros AA, Jacoby GA (1990) Novel plasmid mediated β-lactamases(MIR-1) conferring resistance to oxyimino and α methoxy β-lactams in clinical isolates of Klebsiella pneumoniae. Antimicrob Agents Chemother 34:2200–2209CrossRefPubMedPubMedCentral
17.
go back to reference Black JA, Moland ES, Thomson KS (2005) AmpC disk test for detection of plasmid-mediated AmpC β-lactamases in Enterobacteriaceae lacking chromosomal AmpC β –lactamases. J Clin Microbiol 43:3110–3113CrossRefPubMedPubMedCentral Black JA, Moland ES, Thomson KS (2005) AmpC disk test for detection of plasmid-mediated AmpC β-lactamases in Enterobacteriaceae lacking chromosomal AmpC β –lactamases. J Clin Microbiol 43:3110–3113CrossRefPubMedPubMedCentral
18.
go back to reference Myer K (2001) Methods in biochemical identification of bacteria. Myer’s and Koshi’s manual of diagnostic procedures in medical microbiology and immunology/serology, 2nd ed. Department of Clinical Microbiology, Christian Medical College, Vellore, pp 195–202 Myer K (2001) Methods in biochemical identification of bacteria. Myer’s and Koshi’s manual of diagnostic procedures in medical microbiology and immunology/serology, 2nd ed. Department of Clinical Microbiology, Christian Medical College, Vellore, pp 195–202
19.
go back to reference CLSI; Clinical and Laboratory Standards Institute (2011) Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. CLSI document M100-S21. Clinical and Laboratory Standards Institute, Wayne PA CLSI; Clinical and Laboratory Standards Institute (2011) Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. CLSI document M100-S21. Clinical and Laboratory Standards Institute, Wayne PA
20.
go back to reference Coudron PE (2005) Inhibitor-based methods for detection of plasmid-mediated AmpC beta-lactamases in Klebsiella spp., Escherichia coli and Proteus mirabilis. J Clin Microbiol 43:4163–4167CrossRefPubMedPubMedCentral Coudron PE (2005) Inhibitor-based methods for detection of plasmid-mediated AmpC beta-lactamases in Klebsiella spp., Escherichia coli and Proteus mirabilis. J Clin Microbiol 43:4163–4167CrossRefPubMedPubMedCentral
21.
go back to reference Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145(3):1365–1373PubMedPubMedCentral Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145(3):1365–1373PubMedPubMedCentral
22.
go back to reference MendoncaN LD, Castro AP et al (2006) ctxm-15, oxa-30 and tem-1 producing Escherechia coli in two Portugese regions. J Antimicrob Chemother 57:1014–1016CrossRef MendoncaN LD, Castro AP et al (2006) ctxm-15, oxa-30 and tem-1 producing Escherechia coli in two Portugese regions. J Antimicrob Chemother 57:1014–1016CrossRef
23.
go back to reference Carattoli A, Bertini A, Villa L et al (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228CrossRefPubMed Carattoli A, Bertini A, Villa L et al (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228CrossRefPubMed
24.
go back to reference Sasirekha B, Shivakumar S (2012) Occurrence of plasmid-mediated AmpC b-lactamases among Escherichia coli and Klebsiella pneumoniae clinical isolates in a tertiary care hospital in Bangalore. Indian J Microbiol 52(2):174–179CrossRefPubMed Sasirekha B, Shivakumar S (2012) Occurrence of plasmid-mediated AmpC b-lactamases among Escherichia coli and Klebsiella pneumoniae clinical isolates in a tertiary care hospital in Bangalore. Indian J Microbiol 52(2):174–179CrossRefPubMed
25.
go back to reference Dhanashree B, Mallya SP (2012) Molecular typing of enteropathogenic Escherichia coli from diarrheagenic stool samples. J Clin Diagn Res 6(3):400–404 Dhanashree B, Mallya SP (2012) Molecular typing of enteropathogenic Escherichia coli from diarrheagenic stool samples. J Clin Diagn Res 6(3):400–404
26.
go back to reference Farshad S, Emamghorashi F (2009) The prevalence of virulence genes of E. coli strains isolated from children with urinary tract infection. Saudi J Kidney Dis Transpl 20:613–617PubMed Farshad S, Emamghorashi F (2009) The prevalence of virulence genes of E. coli strains isolated from children with urinary tract infection. Saudi J Kidney Dis Transpl 20:613–617PubMed
27.
go back to reference Kaluzna M, Ferrante P, Sobiczewski P, Scortichini M (2010) Characterization and genetic diversity of pseudomonas syringae from stone fruits and hazelnut using repetitive-pcr and mlst. J Plant Pathol 92:781–787 Kaluzna M, Ferrante P, Sobiczewski P, Scortichini M (2010) Characterization and genetic diversity of pseudomonas syringae from stone fruits and hazelnut using repetitive-pcr and mlst. J Plant Pathol 92:781–787
29.
go back to reference Singhal S, Mathur T, Khan S et al (2005) Evaluation of methods for AmpC β-lactamase in Gram-negative clinical isolates from tertiary care hospitals. Indian J Med Microbiol 23:120–124CrossRefPubMed Singhal S, Mathur T, Khan S et al (2005) Evaluation of methods for AmpC β-lactamase in Gram-negative clinical isolates from tertiary care hospitals. Indian J Med Microbiol 23:120–124CrossRefPubMed
30.
go back to reference Gupta V (2007) An update on newer betalactamases. Indian J Med Res 126(5):417–427PubMed Gupta V (2007) An update on newer betalactamases. Indian J Med Res 126(5):417–427PubMed
31.
go back to reference Ratna AK, Menon I, Kapur I et al (2003) Occurrence and detection of AmpC β-lactamases at a referral hospital in Karnataka. Indian J Med Res 118:29–32PubMed Ratna AK, Menon I, Kapur I et al (2003) Occurrence and detection of AmpC β-lactamases at a referral hospital in Karnataka. Indian J Med Res 118:29–32PubMed
32.
go back to reference Hemalatha PM, Sekar U et al (2007) Detection of AmpC β-lactamases production in Escherichia coli and Klebsiella by an inhibitor based method. Indian J Med Res 126:220–223PubMed Hemalatha PM, Sekar U et al (2007) Detection of AmpC β-lactamases production in Escherichia coli and Klebsiella by an inhibitor based method. Indian J Med Res 126:220–223PubMed
33.
go back to reference Arora S, Bal M (2005) AmpC b-lactamase producing bacterial isolates from Kolkata hospital. Indian J Med Res 122:224–233PubMed Arora S, Bal M (2005) AmpC b-lactamase producing bacterial isolates from Kolkata hospital. Indian J Med Res 122:224–233PubMed
34.
go back to reference Mata C, Miró E, Alvarado A et al (2012) Plasmid typing and genetic context of AmpC βlactamases in Enterobacteriaceae lacking inducible chromosomal AmpC genes: findings from a Spanish hospital 1999–2007. J Antimicrob Chemother 67:115–122CrossRefPubMed Mata C, Miró E, Alvarado A et al (2012) Plasmid typing and genetic context of AmpC βlactamases in Enterobacteriaceae lacking inducible chromosomal AmpC genes: findings from a Spanish hospital 1999–2007. J Antimicrob Chemother 67:115–122CrossRefPubMed
35.
go back to reference Alonso N, Miro E, Pascual V et al (2016) Molecular characterisation of acquired and overproduced chromosomal blaAmpC in Escherichia coli clinical isolates. Int J Antimicrob Agents 47:62–68CrossRefPubMed Alonso N, Miro E, Pascual V et al (2016) Molecular characterisation of acquired and overproduced chromosomal blaAmpC in Escherichia coli clinical isolates. Int J Antimicrob Agents 47:62–68CrossRefPubMed
36.
go back to reference Ahmed SF, Ali MMM, Mohamed ZK et al (2014) Fecal carriage of extended-spectrum β-lactamases and AmpC-producing Escherichia coli in a Libyan community. Ann Clin Microbiol Antimicrob 13:22CrossRefPubMedPubMedCentral Ahmed SF, Ali MMM, Mohamed ZK et al (2014) Fecal carriage of extended-spectrum β-lactamases and AmpC-producing Escherichia coli in a Libyan community. Ann Clin Microbiol Antimicrob 13:22CrossRefPubMedPubMedCentral
37.
go back to reference Sallem RB, Slama KB, Rojo-Bezares B et al (2014) IncI1 Plasmids carrying blaCTX-M-1 or blaCMY-2 genes in Escherichia coli from healthy humans and animals in Tunisia. Microb Drug Resist. doi:10.1089/mdr.2013.0224 PubMed Sallem RB, Slama KB, Rojo-Bezares B et al (2014) IncI1 Plasmids carrying blaCTX-M-1 or blaCMY-2 genes in Escherichia coli from healthy humans and animals in Tunisia. Microb Drug Resist. doi:10.​1089/​mdr.​2013.​0224 PubMed
38.
go back to reference Galán-Sánchez F, Aznar-Marín P, Marín-Casanova P et al (2014) Diversity of bla genes and low incidence of CTX-M in plasmid-mediated AmpC-producing Escherichia coli clinical isolates. APMIS 122(9):796–799CrossRefPubMed Galán-Sánchez F, Aznar-Marín P, Marín-Casanova P et al (2014) Diversity of bla genes and low incidence of CTX-M in plasmid-mediated AmpC-producing Escherichia coli clinical isolates. APMIS 122(9):796–799CrossRefPubMed
39.
go back to reference Bajaj P, Singh NS, Kanaujia PK et al (2015) Distribution and molecular characterization of genes encoding CTX-M and AmpC β-lactamases in Escherichia coli isolated from an Indian urban aquatic environment. Sci Total Environ 505:350–356CrossRefPubMed Bajaj P, Singh NS, Kanaujia PK et al (2015) Distribution and molecular characterization of genes encoding CTX-M and AmpC β-lactamases in Escherichia coli isolated from an Indian urban aquatic environment. Sci Total Environ 505:350–356CrossRefPubMed
40.
go back to reference Ibrahim DR, Dodd CE, Stekel DJ et al (2016) Multidrug resistant, extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiol Ecol 92 10.1093/femsec/fiw01 CrossRef Ibrahim DR, Dodd CE, Stekel DJ et al (2016) Multidrug resistant, extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiol Ecol 92 10.​1093/​femsec/​fiw01 CrossRef
Metadata
Title
Emergence of co-production of plasmid-mediated AmpC beta-lactamase and ESBL in cefoxitin-resistant uropathogenic Escherichia coli
Authors
B. Ghosh
M. Mukherjee
Publication date
01-09-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 9/2016
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-016-2683-z

Other articles of this Issue 9/2016

European Journal of Clinical Microbiology & Infectious Diseases 9/2016 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.