Abstract
Antibiotic resistance among members of the family Enterobacteriaceae was prospectively surveyed by eight French private laboratories over a 5-month period in 1999. A total of 2,599 consecutive and nonduplicate strains were collected, mainly (60.9%) from patients in the community. Most strains (82.9%) derived from urine. Escherichia coli was the predominant (73.9%) organism isolated. The overall rates of antibiotic resistance were as follows: amoxicillin, 53.4%; amoxicillin-clavulanic acid, 27.3%; ticarcillin, 44.2%; piperacillin-tazobactam, 3.2%; cephalothin, 29.2%; cefuroxime, 14.7%; cefoxitin, 11.5%; ceftazidime, 3.6%; cefotaxime, 2.8%; cefepime, 0.3%; imipenem, 0.1%; gentamicin (G), 3.8%; tobramycin (T), 5.0%; netilmicin (Nt), 3.7%; amikacin (A), 0.7%; nalidixic acid, 14.3%; ofloxacin, 10.4%; cotrimoxazole, 21.1%; nitrofurantoin, 12.7%; fosfomycin, 5.2%; tetracycline, 50.1%; and colistin, 12.5%. Beta-lactam resistance phenotypes essentially comprised penicillinase production (33.9%), overexpression of chromosomal cephalosporinase (4.6%), and synthesis of inhibitor-resistant TEM/OXA enzymes (1.5%) or extended-spectrum β-lactamases (1.5%). Aminoglycoside resistance phenotypes consisted of GTNt (93 strains), TNtA (68 strains), GTNtA (14 strains), T (4 strains), GT (3 strains), G (1 strain), and reduced uptake/permeability (3 strains). Most of the nalidixic acid-resistant strains were resistant to ofloxacin (72.8%). Antibiotic resistance rates and phenotypes varied widely according to the bacterial group and the source of the strains. Significantly higher rates were observed in private healthcare centers than in the community, due to a higher proportion of both resistant species and resistant strains. However, multidrug-resistant isolates, including five extended-spectrum β-lactamase-producing strains, were also recovered from the community.
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Péan Y, Goldstein FW, Guerrier ML, De Bels F, les membres de VIGIL’ROC (1999) Sensibilité aux β-lactamines des bactéries isolées en ville et à l’hôpital au cours d’une enquête multicentrique française. Antibiotiques 1:165–170
Robert J, Cambau E, Grenet K, Trystram D, Péan Y, Fiévet MH, Jarlier V (2001) Trends in quinolone susceptibility of Enterobacteriaceae among inpatients of a large university hospital: 1992–98. Clin Microbiol Infect 7:553–561
Sirot J, Nicolas-Chanoine MH, Chardon H, Avril JL, Cattoen C, Croix JC, Dabernat H, Fosse T, Ghnassia JC, Lecaillon E, Marmonier A, Roussel-Delvallez M, Soussy CJ, Trevoux A, Vandenesch F, Dib C, Moniot-Ville N, Rezvani Y (2002) Susceptibility of Enterobacteriaceae to β-lactam agents and fluoroquinolones: a 3-year survey in France. Clin Microbiol Infect 8:207–213
Arzouni JP, Bouilloux JP, De Moüy D, Fleutiaux S, Galinier J, Gayon A, Lacharme H, Larribet G, Lepargneur JP (2000) Les infections urinaires chez la femme de 15 à 65 ans en pratique de ville: surveillance de la sensibilité de Escherichia coli à la fosfomycine trométanol en fonction des antécédents. Méd Mal Infect 30:699–702
De Moüy D, Berges JL, Bouilloux JP, Charbit N, Fischer I, Grobost F, Larribet G, Porcher T (1997) Sensibilité à la fosfomycine des principales bactéries issues d’infections urinaires observées en pratique de ville chez les femmes de 15 à 65 ans. Méd Mal Infect 27:903–906
De Moüy D, Cavallo JD, Armengaud A, et des membres de l’Aforcopi-Bio (1998) Escherichia coli et infections urinaires en pratique de ville: étude en fonction des antécédents d’hospitalisation et de traitement antibiotique. BEH 24:105
De Moüy D, Cavallo JD, Armengaud M, Arzouni JP, Berges JL, Bouilloux JP, Charbit N, Cirioni N, Fabre R, Garrabe E, Galinier J, Gayon A, Grobost F, Larribet G, Lepargneur JP (1999) Infections urinaires en pratique de ville: étiologies et sensibilité aux antibiotiques en fonction des antécédents. Presse Med 28:1624–1628
De Moüy D, Cavallo JD, Fabre R, Garrabe E, Grobost F, Armengaud M, Labia R, et les membres de l’Aforcopibio (1997) Les entérobactéries isolées d’infections urinaires en pratique de ville: étude AFORCOPIBIO. Méd Mal Infect 27:642–645
Goldstein FW, and the Multicentre Study Group (2000) Antibiotic susceptibility of bacterial strains isolated from patients with community-acquired urinary tract infections in France. Eur J Clin Microbiol Infect Dis 19:112–117
Observatoire National de l’Epidémiologie de la Résistance des Bactéries aux Antibiotiques (ONERBA) (2000) Facteurs influant sur la fréquence et sur le niveau de sensibilité aux antibiotiques des souches d’Escherichia coli et Proteus mirabilis isolées au cours des infections urinaires chez les patients ambulatoires. Méd Mal Infect 30:714–720
Bradley SF (1999) Issues in the management of resistant bacteria in long-term-care facilities. Infect Control Hosp Epidemiol 20:362–366
Nicolle LE, Strausbaugh LJ, Garibaldi RA (1996) Infections and antibiotic resistance in nursing homes. Clin Microbiol Rev 9:1–17
Vromen M, Van der Ven AJAM, Knols A, Stobberingh EE (1999) Antimicrobial resistance patterns in urinary isolates from nursing home residents. Fifteen years of data reviewed. J Antimicrob Chemother 44:113–116
Courvalin P (1992) Interpretive reading of antimicrobial susceptibility tests. ASM News 58:368–375
Livermore DM (1995) β-lactamases in laboratory and clinical resistance. Clin Microbiol Rev 8:557–584
Livermore DM, Winstanley TG, Shannon KP (2001) Interpretative reading: recognizing the unusual and inferring resistance mechanisms from resistance phenotypes. J Antimicrob Chemother 48 (Suppl S1):87–102
De Champs C, Sirot D, Chanal C, Bonnet R, Sirot J, and the French Study Group (2000) A 1998 survey of extended-spectrum β-lactamases in Enterobacteriaceae in France. Antimicrob Agents Chemother 44:3177–3179
Henquell C, Sirot D, Chanal C, De Champs C, Chatron P, Lafeuille B, Texier P, Sirot J, Cluzel R (1994) Frequency of inhibitor-resistant TEM β-lactamases in Escherichia coli isolates from urinary tract infections in France. J Antimicrob Chemother 34:707–714
Jarlier V, Nordmann P (2000) Entérobactéries et β-lactamines. In: Freney J, Renaud F, Hansen W, Bollet C (eds) Précis de bactériologie clinique. ESKA, Paris, pp 649–665
Leflon-Guibout V, Speldooren V, Heym B, Nicolas-Chanoine MH (2000) Epidemiological survey of amoxicillin-clavulanate resistance and corresponding molecular mechanisms in Escherichia coli isolates in France: new genetic features of bla TEM genes. Antimicrob Agents Chemother 44:2709–2714
Wiener J, Quinn JP, Bradford PA, Goering RV, Nathan C, Bush K, Weinstein RA (1999) Multiple antibiotic-resistant Klebsiella and Escherichia coli in nursing homes. JAMA 281:517–523
Cormican M, Morris D, Corbett-Feeeney G, Flynn J (1998) Extended spectrum β-lactamase production and fluoroquinolone resistance in pathogens associated with community acquired urinary tract infection. Diagn Microbiol Infect Dis 32:317–319
Hryniewicz K, Szczypa K, Sulikowska A, Jankowski K, Betlejewska K, Hryniewicz W (2001) Antibiotic susceptibility of bacterial strains isolated from urinary tract infections in Poland. J Antimicrob Chemother 47:773–780
Comité de l’Antibiogramme de la Société Française de Microbiologie (2003) Communiqué 2003.http://www.sfm.asso.fr. Cited March 2003
Lambert T, Courvalin P (2000) Entérobactéries et aminosides. In: Freney J, Renaud F, Hansen W, Bollet C (eds) Précis de bactériologie clinique. ESKA, Paris, pp 666–677
Miller GH, Sabatelli FJ, Hare RS, Glupczynski Y, Mackey P, Shlaes D, Shimizu K, Shaw KJ, and the Aminoglycoside Resistance Study Groups (1997) The most frequent aminoglycoside resistance mechanisms—changes with time and geographic area: a reflection of aminoglycoside usage patterns? Clin Infect Dis 24 (Suppl 1):46–62
Jones RN (1998) Important and emerging β-lactamase-mediated resistances in hospital-based pathogens: the Amp C enzymes. Diagn Microbiol Infect Dis 31:461–466
Sanders WE, Sanders CC (1997) Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin Microbiol Rev 10:220–241
Gheorghiu R, Yuan M, Hall LMC, Livermore DM (1997) Bases of variation in resistance to β-lactams in Klebsiella oxytoca isolates hyperproducing K1 β-lactamase. J Antimicrob Chemother 40:533–541
Chaïbi EB, Sirot D, Paul G, Labia R (1999) Inhibitor-resistant TEM β-lactamases: phenotypic, genetic and biochemical characteristics. J Antimicrob Chemother 43:447–458
Arpin C, Labia R, Dubois V, Noury P, Souquet M, Quentin C (2002) TEM-80, a novel inhibitor-resistant β-lactamase in a clinical isolate of Enterobacter cloacae. Antimicrob Agents Chemother 46:1183–1189
Nordmann P (1998) Trends in β-lactam resistance among Enterobacteriaceae. Clin Infect Dis 27 (Suppl 1):100–106
Bermudes H, Arpin C, Jude F, El-Harrif Z, Bébéar C, Quentin C (1997) Molecular epidemiology of an outbreak due to extended-spectrum β-lactamase-producing enterobacteria in a French hospital. Eur J Clin Microbiol Infect Dis 16:523–529
Gniadkowski M (2001) Evolution and epidemiology of extended-spectrum β-lactamases (ESBLs) and ESBL-producing microorganisms. Clin Microbiol Infect 7:597–608
Arpin C, Coze C, Rogues AM, Gachie JP, Bébéar C, Quentin C (1996) Epidemiological study of an outbreak due to multidrug-resistant Enterobacter aerogenes in a medical intensive care unit. J Clin Microbiol 34:2163–2169
Bosi C, Davin-Regli A, Bornet C, Mallea M, Pages JM, Bollet C (1999) Most Enterobacter aerogenes strains in France belong to a prevalent clone. J Clin Microbiol 37:2165–2169
Hernández-Allés S, Benedí VJ, Martínez-Martínez L, Pascual Á, Aguilar A, Tomás JM, Albertí S (1999) Development of resistance during antimicrobial therapy caused by insertion sequence interruption of porin genes. Antimicrob Agents Chemother 43:937–939
Arpin C, Dubois V, Coulange L, André C, Fischer I, Noury P, Grobost F, Brochet J-P, Jullin J, Dutilh B, Larribet G, Lagrange I, Quentin C (2003) Extended-spectrum ß-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob Agents Chemother 47:3506–3514
Bornet C, Davin-Regli A, Bosi C, Pages JM, Bollet C (2000) Imipenem resistance of Enterobacter aerogenes mediated by outer membrane permeability. J Clin Microbiol 38:1048–1052
Acar JF, Goldstein FW (1997) Trends in bacterial resistance to fluoroquinolones. Clin Infect Dis 24 (Suppl 1):67–73
Bird J, Browning R, Hobson RP, MacKenzie FM, Brand J, Gould IM (1998) Multiply-resistant Klebsiella pneumoniae: failure of spread in community-based elderly care facilities. J Hosp Infect 40:243–247
Rice LB, Eckstein EC, DeVente J, Shlaes DM (1996) Ceftazidime-resistant Klebsiella pneumoniae isolates recovered at the Cleveland Department of Veterans Affairs medical center. Clin Infect Dis 23:118–124
Rice LB, Willey SH, Papanicolaou GA, Medeiros AA, Eliopoulos GM, Moellering RC, Jacoby GA (1990) Outbreak of ceftazidime resistance caused by extended-spectrum β-lactamases at a Massachusetts chronic-care facility. Antimicrob Agents Chemother 34:2193–2199
Bradford PA, Urban C, Jaiswal A, Mariano N, Rasmussen BA, Projan SJ, Rahal JJ, Bush K (1995) SHV-7, a novel cefotaxime-hydrolyzing β-lactamase, identified in Escherichia coli isolates from hospitalized nursing home patients. Antimicrob Agents Chemother 39:899–905
Rasmussen BA, Bradford PA, Quinn JP, Wiener J, Weinstein RA, Bush K (1993) Genetically diverse ceftazidime-resistant isolates from a single center: biochemical and genetic characterization of TEM-10 β-lactamases encoded by different nucleotide sequences. Antimicrob Agents Chemother 37:1989–1992
Heseltine P (2000) Has resistance spread to the community? Clin Microbiol Infect 6 (Suppl 2):11–16
Gupta K, Hooton TM, Stamm WE (2001) Increasing antimicrobial resistance and the management of uncomplicated community-acquired urinary tract infections. Ann Intern Med 135:41–50
Acknowledgements
The authors are grateful to the I2A Company for lending the SIRscan system during the study period. This work was supported by grants from Bristol-Myers Squibb, Glaxo Wellcome, MSD-Chibret, Roussel Diamant, SmithKline Beecham, and Wyeth Léderlé Companies, France. The experiments comply with the current French laws.
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Quentin, C., Arpin, C., Dubois, V. et al. Antibiotic Resistance Rates and Phenotypes Among Isolates of Enterobacteriaceae in French Extra-Hospital Practice. Eur J Clin Microbiol Infect Dis 23, 185–193 (2004). https://doi.org/10.1007/s10096-003-1081-5
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DOI: https://doi.org/10.1007/s10096-003-1081-5