Carriage of Beta-Lactamase-Producing Enterobacteriaceae Among
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International Journal of Infectious Diseases 45 (2016) 24–31 Contents lists available at ScienceDirect International Journal of Infectious Diseases jou rnal homepage: www.elsevier.com/locate/ijid Carriage of beta-lactamase-producing Enterobacteriaceae among nursing home residents in north Lebanon Iman Dandachi, Elie Salem Sokhn, Elie Najem, Eid Azar, Ziad Daoud * Faculty of Medicine and Medical Sciences, Clinical Microbiology Laboratory, University of Balamand, PO Box 33, Amioun, Beirut, Lebanon A R T I C L E I N F O S U M M A R Y Article history: Background: Multidrug-resistant (MDR) Enterobacteriaceae can cause severe infections with high Received 15 December 2015 morbidity, mortality, and health care costs. Individuals can be fecal carriers of these resistant organisms. Received in revised form 18 January 2016 Data on the extent of MDR Enterobacteriaceae fecal carriage in the community setting in Lebanon are very Accepted 10 February 2016 scarce. The aim of this study was to investigate the fecal carriage of MDR Enterobacteriaceae among the Corresponding Editor: Eskild Petersen, elderly residents of two nursing homes located in north Lebanon. Aarhus, Denmark. Methods: Over a period of 4 months, five fecal swab samples were collected from each of 68 elderly persons at regular intervals of 3–4 weeks. Fecal swabs were subcultured on selective media for the Keywords: screening of resistant organisms. The phenotypic detection of extended-spectrum beta-lactamase Carriage (ESBL), AmpC, metallo-beta-lactamase (MBL), and Klebsiella pneumoniae carbapenemase (KPC) Nursing homes production was performed using the beta-lactamase inhibitors ethylenediaminetetraacetic acid, Resistance phenylboronic acid, and cloxacillin. A temocillin disk was used for OXA-48. Multiplex PCRs were used for Carbapenemases the genotypic detection of ESBL and carbapenemase genes, and sequencing was performed to identify ESBLs CTX-M-15. The medical records of each subject were reviewed on a regular basis in order to assess the risk factors associated with MDR Enterobacteriaceae fecal carriage. Results: Over the study period, 76.5% of the recruited elderly persons were at least one-time carriers. A total of 178 isolates were obtained. Phenotypic testing revealed that 91.5% of them were ESBL producers, 4% were AmpC producers, 2.8% were co-producers of ESBL and AmpC, and 1.7% were co-producers of OXA-48 and ESBL. Recent antibiotic intake was found to be the only independent risk factor associated with the fecal carriage of MDR Enterobacteriaceae. Conclusions: The high prevalence of MDR Enterobacteriaceae detected in this study and the emergence of carbapenem resistance is alarming. Efficient infection control measures and antibiotic stewardship programs are urgently needed in these settings in order to limit the spread of resistant strains. ß 2016 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). of these cases is often challenging due to the limited therapeutic 1. Introduction options; the antibiotic pipeline is drying up and no new antimicrobial agents targeted against MDR Enterobacteriaceae Multidrug-resistant (MDR) Enterobacteriaceae are currently 6 1,2 are foreseen in the near future. considered a major public health concern worldwide. They 3 There is increasing evidence that nursing homes in the can be transmitted easily among patients and healthy persons. community are important reservoirs for MDR Enterobacteria- Studies have shown that after being selected by antibiotics, the 4,7 ceae. This is in major part due to the inappropriate use of cross-transmission of these organisms occurs frequently in the 8 4 antimicrobial agents in these facilities, in addition to the health care setting. This dissemination will eventually lead to difficulties particularly faced when establishing antibiotic stew- increased rates of MDR Enterobacteriaceae carriage. This carriage is 9,10 ardship and infection control programs. The prevalence of MDR often unrecognized and has been known to increase the risk of 5 Enterobacteriaceae colonization in nursing homes varies according contracting infections caused by resistant agents. The treatment to the geographical location, patient population, and the level of 10 care provided. In the Middle East, although several studies have been * Corresponding author. Tel./fax: +961.6.930250 (ext. 3819). E-mail address: [email protected] (Z. Daoud). conducted to assess the prevalence of MDR Enterobacteriaceae in http://dx.doi.org/10.1016/j.ijid.2016.02.007 1201-9712/ß 2016 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). I. Dandachi et al. / International Journal of Infectious Diseases 45 (2016) 24–31 25 11 the hospital ward, data on the prevalence of MDR Enterobacter- incontinence, the presence of wounds or ulcers, and the previous or iaceae among nursing home residents in these countries are very current use of a urinary catheter were also reported. Furthermore, scarce. In Lebanon, clinical investigations have shown that the the recruited elderly persons were checked for comorbidities (MDR 12 prevalence of MDR Enterobacteriaceae is on a continuous rise. bacterial infections, diabetes, cancer, pulmonary, cardiovascular, Local data reported in the form of flyers summarizing the renal, or neurological diseases, and urogenital pathologies), susceptibility of bacteria at the Centre Hospitalier Du Nord in hospital admission during the last year, and whether they had the north of Lebanon, show that between 2011 and 2013 the rate of undergone any surgeries, as well as their antibiotic intake during extended-spectrum beta-lactamase (ESBL) production among the last 3 months. clinical isolates increased from 24.6% to 30.4% and from 26.5% to 31.7% in Escherichia coli and Klebsiella pneumoniae, respectively 2.4. Collection of fecal swabs and isolation of resistant (Ziad Daoud). Another recent study reported an increase of 1.2% in Enterobacteriaceae resistance and decreased susceptibility to ertapenem in clinical isolates of Enterobacteriaceae. This resistance was mainly attribut- Between December 2013 and April 2014, five samples (fecal 12 ed to the production of OXA-48 beta-lactamase. swabs) were obtained from each of 68 elderly persons at regular In an attempt to understand the situation of carriage in the intervals of 3–4 weeks. A total of 262 samples were collected: 59 at nursing homes of the country and to shed light on this important collection 1, 51 at collection 2, 57 at collection 3, 51 at collection 4, issue, the present research group conducted a study in Lebanon in and 44 at collection 5. The fecal swabs were subcultured on which it was found that 71.6% of the recruited elderly subjects MacConkey agar supplemented with cefotaxime (2 mg/ml) for the 13 were at least one-time carriers during the study period. The plan screening of MDR Enterobacteriaceae. From each selective plate, was to study the situation in the north of Lebanon, where the different colonies presenting with different morphologies were extent of the spread of bacterial resistance in the community is not picked up separately and suspended in Luria broth. After overnight well documented. The socio-cultural as well as economic and incubation, each bacterial suspension was subcultured again on a educational levels in the north of Lebanon are also very particular selective plate. The following day, if the plate contained colonies to this area of the country. These include the level of poverty and with single morphologies, the isolate was preserved in 20% glycerol the absence of basic governmental services such as public aliquots at À20 8C for further testing; if more than one type was sanitation and infrastructure, as most of the services are observed, a re-isolation was performed for further purification. concentrated in the capital Beirut. Unfortunately, all of these data An elderly subject was defined as a carrier if an MDR are anecdotal and based on impressions, since official statistics are Enterobacteriaceae was isolated from his/her fecal sample. If the not available in the country. patient was found to be a carrier at all five collections, he/she was The aim of this study was thus to investigate the fecal carriage considered a ‘permanent carrier’. If the resistant bacterium was of MDR Enterobacteriaceae among the residents of two major isolated at fewer than five collections, the subject was defined as an nursing homes located in the north of Lebanon through the ‘intermittent carrier’. Finally, if no MDR Enterobacteriaceae was determination of the prevalence, dynamics, and risk factors for isolated during the five collections, the subject was considered a MDR Enterobacteriaceae fecal carriage among elderly subjects. In ‘never carrier’. All isolates were identified using biochemical addition, it was sought to determine whether CTX-M-15, the gallery tests (API 20E; bioMe´rieux). 14 predominant ESBL gene in the Lebanese population, was also the major ESBL genotype carried among these elderly people. 2.5. Phenotypic tests 2. Materials and methods Antimicrobial susceptibility testing was performed for 178 iso- lates using the Kirby–Bauer disk diffusion method. Interpretation 2.1. 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