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And/Or Extended-Spectrum (ESBL) ß-Lactamase- Producing Proteus Spp

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And/Or Extended-Spectrum (ESBL) ß-Lactamase- Producing Proteus Spp ORIGINAL ARTICLE Molecular epidemiology and antimicrobial susceptibility of AmpC- and/or extended-spectrum (ESBL) ß-lactamase- producing Proteus spp. clinical isolates in Zenica-Doboj Canton, Bosnia and Herzegovina Selma Uzunović1, Amir Ibrahimagić1, Branka Bedenić2,3 1Department for Laboratory Diagnostics, Institute for Public Health and Food Safety, 2School of Medicine, University of Zagreb, 3Clinical Department of Clinical and Molecular Microbiology, University Hospital Center Zagreb; Zagreb, Croatia ABSTRACT Aim To investigate prevalence, antimicrobial susceptibility, mo- lecular characteristics, and genetic relationship of AmpC- and/ or extended spectrum beta lactamase (ESBL)- producing Proteus spp. clinical isolates in Zenica-Doboj Canton, Bosnia and Herze- govina. Methods Antibiotic susceptibility was determined by disc diffusi- on and broth microdilution methods according to CLSI guideli- nes. Double-disk synergy test was performed in order to screen for ESBLs, and combined disk test with phenylboronic acid to detect AmpC β -lactamases. PCR was used to detect blaESBL/blacarb genes. Genetic relatedness of the strains was determined by pulsed-field- gel-electrophoresis (PFGE). Corresponding author: Results Eleven ESBL-producing isolates were included in the Amir Ibrahimagić study (six inpatients and five outpatients). Susceptibility rate to Department of Laboratory Diagnostics, amoxicillin-clavulanic acid, imipenem and meropenem was 100%. Resistance rate to cefuroxime was 100%, gentamicine 90.9%, pi- Institute for Public Health and Food Safety peracillin/tazobactam 81.8%, cefotaxim, ceftriaxone and ceftazi- Zenica dime 72.7%, cefoxitine and ciprofloxacine 63.6% and to cefepime Fra Ivana Jukića 2, 72000 Zenica, 45.5%. In five (out of 11) isolates multi-drug resistance (MDR) to Bosnia and Herzegovina cephalosporins, cefamicines, amynocligosides and fluoroquinolo- Phone: +387 32 443 580; nes was detected. Besides TEM-1 which was detected in all iso- Fax: +387 32 443 530; lates, CTX-M+OXA-1 β-lactamases were detected in seven (out of 11; 63.6%) isolates (five bla and two bla genes), E-mail: [email protected] CTX-M-1 CTX-M-15 and CMY-2 β-lactamase in two isolates. PFGE showed no genetic relatedness. Conclusion Because of high prevalence of MDR strains in epide- Original submission: miologically unrelated patients with AmpC- and/or ESBL produ- 14 March 2016; cing Proteus spp. infection, further surveillance is needed. Mole- Accepted: cular characterization and strain typing, or at least phenotypic test 04 April 2016. for AmpC/ESBL production is important for appropriate therapy doi: 10.17392/853-16 and the detection of sources and modes of spread, which is the main step in order to design targeted infection control strategies. Key words: ESBL, CMY-2, antimicrobial resistance Med Glas (Zenica) 2016; 13(2):103-112 103 Medicinski Glasnik, Volume 13, Number 2, August 2016 INTRODUCTION β-lactamases have been detected among isolates from Iran (1), France (2), Saudi Arabia (14), Italy Proteus spp. cause various human infections and (15), and Japan (16). it was firstly documented as extended-spectrum beta-lactamase (ESBL)-producer in 1987 (1). Pro- Investigations of molecular characteristics and teus spp. were susceptible to beta (β)-lactam anti- epidemiology of β-lactamase producing Proteus biotics (2), but progressive increase of resistance spp. in Bosnia and Herzegovina (B&H) are scar- to beta-lactam antibiotics mediated by the produc- ce. TEM, CTX-M and AmpC genes have been tion of acquired beta-lactamases has occurred (3). recently reported in Gram-negative bacteria, Extended-spectrum β -lactamases showing acti- including Proteus spp., causing urinary tract in- vity to extended-spectrum cephalosporins have fections in Zenica-Doboj Canton (17). also started to spread, including most frequently The aim of the study was to investigate molecular TEM-type derivatives, but also other enzymes (4). epidemiology and genetic relatedness of AmpC Numerous outbreaks of infections with organisms β-lactamase- and ESBL-producing Proteus spp. producing ESBLs have been observed in many inpatient and outpatient isolates, as well as their countries (5-7). Resistance to beta-lactam drugs antimicrobial susceptibility. is caused by chromosomal and plasmid encoded enzymes (5). Horizontal acquisition of AmpC MATERIALS AND METHODS β -lactamases represents an important driver of Setting, bacterial isolates and study design increasing resistance in Europe, and it is associated with the clonal expansion of resistant strains (8). During the period December 2009 - May 2010, The organism has achieved ability to cause infecti- the total of 9092 and 16037 samples from the ons leading to prolonged hospital stay, an increase inpatients and outpatients, respectively, were of morbidity and mortality, and consequently an collected at the Microbiology Laboratory of the increase of health care associated costs (9). Cantonal Hospital Zenica. Among inpatients, ESBL-producing Gram-negative isolates are re- Gram-negative bacteria were isolated from 1254 sistant to extended-spectrum cephalosporins and (72.7%) samples, of which ESBL and/or AmpC monobactams, except cefamycins, carbapenems, β-lactamase producing bacteria were detected in and β-lactam/ β-lactamase inhibitors; AmpC be- 126 (out of 1254, 10%) samples; Proteus spp. ta-lactamases producing isolates are resistant to were isolated from 201 (out of 1254, 16.0%) penicillins, cephalosporins, cephamycins, mono- samples, of which 27 (out of 201; 13.4%) were bactams and β-lactam/β-lactamase inhibitor, but ESBL and/or AmpC β-lactamase producing iso- usually sensitive to carbapenems (10). Proteus lates. Among outpatients, Gram-negative bac- spp. are intrinsically resistant to nitrofuranto- teria were isolated from 2857 (80.9%) samples, in and tetracycline. Although Proteus spp. are of which 184 (6.4%) were ESBL- and/or AmpC intrinsically susceptible to aminoglycosides, β-lactamase producing bacteria; Proteus spp. fluoroquinolones, and trimethoprim-sulfamet- were isolated from 365 (out of 2857; 12.8%) hoxazole, co-resistance to these drugs has been samples, of which 26 (out of 365; 7.1%) were frequently reported among ESBL-producing β-lactamase producing isolates. Proteus spp. isolates, and the treatment is often Among 53 ESBL- and /or AmpC β-lactamase- limited to carbapenems (11). Reportedly, suscep- producing Proteus spp. (27 in- and 26 outpati- tibility of Proteus spp. to β-lactam/β-lactamase ents), 11 (six inpatient and five outpatient) were inhibitors, ciprofloxacin, and third generation available for further analysis. cephalosporins varies widely, 74- 94%, 60- 90%, Institutional review board approval from the Et- and 90- 99%, respectively, depending on pati- hics Committee of the Cantonal Hospital Zenica ents’ age, gender, hospital department, duration was obtained prior to the initiation of the study. of hospitalization and infection type (12). The ESBLs commonly reported among Pro- Antimicrobial susceptibility testing teus spp. are TEM and CTX-M, while other ESBLs (SHV, TEM β-lactamase inhibitors) Susceptibility testing to 12 antimicrobials was are less frequent (13). TEM, CTX-M and other performed by a twofold microdilution technique 104 Uzunović et al. AmpC and ESBL producing Proteus spp. according to CLSI (Clinical and Laboratory screened for production of AmpC β -lactamases by Standards Institute) standard procedure (18): combined disk test using 3-amino phenylboronic amoxycillin+clavulanic acid (AMC), cefazolin acid (PBA) (Sigma-Aldrich, Steinheim, Germany). (CZ), cefuroxime (CXM), ceftazidime (CAZ), The stock solution was prepared as previously re- cefotaxime (CTX), ceftriaxone (CRO), cefoxi- commended (19) by dissolving PBA (benzenebo- tin (FOX), cefepime (FEP), imipenem (IMP), ronic acid; Sigma-Aldrich, Steinheim, Germany) in meropenem (MEM), gentamicin (GM), and ci- dimethyl sulfoxide at a concentration of 20 mg/mL. profloxacin (CIP). The following MIC resistan- 20 μL (containing 400 μg of boronic acid) of the so- ce breakpoints were used: ≥32 for amoxicillin/ lution was dispensed onto antibiotic disks. The dis- clavulanic, cefazolin, cefuroxime, ceftazidime, ks were then dried and used within 60 min. The te- cefoxitime and cefepime; ≥64 for cefotaxime and sts were performed by inoculating Mueller-Hinton ceftriaxone; ≥16 for imipenem and meropenem; agar by the standard diffusion method and placing ≥8 for gentamicine; and ≥4 for ciprofloxacin. E. disks containing four different β-lactams (CAZ, 10 coli ATCC 25922 (ESBL negative) and K. pne- µg; CRO, 30 µg; CTX, 5 µg; FEP, 30 µg) with or umoniae 700603 (ESBL positive) were used as without boronic acid onto the agar. The agar plates quality control strains. were incubated at 37°C overnight. The diameter of the growth-inhibitory zone around a β-lactam disk Detection of ESBLs, AmpC beta-lactamases and with boronic acid was compared with that around carbapenemases the corresponding β-lactam disk without boronic ESBL production was determined by double- acid. The test was considered positive for the detec- disk-synergy test (DDST). Overnight broth cul- tion of AmpC production when the diameter of the ture of test strain was diluted in saline, adjusted growth-inhibitory zone around a β-lactam disk with to McFarland standard suspension 0.5 and inocu- boronic acid was ≥5 mm larger than that around a lated onto Mueller-Hinton agar (MH); disk con- disk containing the β-lactam substrate alone (20). taining amoxicillin/clavulanate (20/10 µg) was Production
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