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Abstract
Antibiotic resistance and especially multiresistance in Enterococci, is a serious public health issue especially in infections of immunocompromised patients. EfrAB is a heterodimeric multidrug ATP-binding cassette (ABC) transporter that causes endogenous resistance to antimicrobials including fluoroquinolones in Enterococcus spp. The aim of this study was to seek the gene expression rate and role of efrAB efflux pump in ciprofloxacin resistant Enterococcus faecalis and Multilocus Sequence Typing (MLST) of multiresistant isolates. Phenotypic and genotyping identification of 80 E. faecalis isolates were performed. Minimum inhibitory concentrations (MICs) to ciprofloxacin (CIP) were measured with and without carbonylcyanide 3-chlorophenylhydrazone (CCCP) by broth microdilution. After DNA extraction and sequencing for detection of efrA and efrB genes, the efrAB efflux positive isolates that were resistant to ciprofloxacin and showed decrease of ciprofloxacin MIC range were identified. Isolates that exhibited decrease in ciprofloxacin MIC range from two to ten folds were assessed for biofilm formation and finally, the expression levels of efrB, efrA genes were measured by quantitative Real-Time PCR (qRT-PCR). High rates of resistance to tetracycline and minocycline and low rates of resistance to the most antibiotics used in this study were detected. The results in this study indicated that the incidence of Multiple drug resistance (MDR) was 23.7% and all isolates that were resistant to ciprofloxacin revealed several degrees of overexpression in efrA and efrB genes. Our study found two ST480 and one ST847 in E. faecalis isolates. In conclusion, despite of low frequency of resistance to the most antibiotics and MDRs in our region, we found one ST480 isolate with resistance to eight antibiotics that also exists in other parts of the world.
-
[1]
Kitagawa K, Shigemura K, Yamamichi F, Alimsardjono L, Rahardjo D, Kuntaman K, et al.. International comparison of causative bacteria and antimicrobial susceptibilities of urinary tract infections between Kobe, Japan and Surabaya, Indonesia. JJID 2017; 71: 8–13.
-
[2]
Sharma D, Preston SE, Hage R. Emerging antibiotic resistance to bacterial isolates from human urinary tract infections in Grenada. Cureus 2019; 11: e5752.
-
[3]
Defoirdt T, Sorgeloos P, Bossier P. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 2011; 14: 251–8.
-
[4]
Lee EW, Huda MN, Kuroda T, Mizushima T, Tsuchiya T. EfrAB, an ABC multidrug efflux pump in Enterococcus faecalis. Antimicrob Agents Chemother 2003; 47: 3733–8.
-
[5]
Shepard BD, Gilmore MS. Antibiotic-resistant enterococci: the mechanisms and dynamics of drug introduction and resistance. Microb Infect 2002; 4: 215–24.
-
[6]
Pesavento G, Calonico C, Ducci B, Magnanini A, Nostro AL. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol 2014; 41: 1–7.
-
[7]
Conceição N, Oliveira CdCHB, Silva PRd, Ávila BGM, Oliveir AGd. Trends in antimicrobial resistance among clinical isolates of enterococci in a Brazilian tertiary hospital: a 4-year study. Rev Soc Bras Med Tro 2011; 44: 177–81.
-
[8]
Yasufuku T, Shigemura K, Shirakawa T, Matsumoto M, Nakano Y, Tanaka K, et al. Mechanisms of and risk factors for fluoroquinolone resistance in clinical Enterococcus faecalis isolates from patients with urinary tract infections. J Clin Microbiol 2011; 49: 3912–16.
-
[9]
Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP. Emerging resistance among bacterial pathogens in the intensive care unit – a European and North American Surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 2004; 3: 14.
-
[10]
Giannakopoulos X, Sakkas H, Ragos V, Tsiambas E, Bozidis P, Evangelou AM, et al.. Impact of enterococcal urinary tract infections in immuno-compromised–neoplastic patients. J BUON 2019; 24: 1768–75.
-
[11]
El Khoury J, Fishman J. Linezolid in the treatment of vancomycin‐resistant Enterococcus faecium in solid organ transplant recipients: report of a multicenter compassionate‐use trial. Transpl Infect Dis 2003; 5: 121–5.
-
[12]
Barbosa J, Ferreira V, Teixeira P. Antibiotic susceptibility of enterococci isolated from traditional fermented meat products. Food Microbiol 2009; 26: 527–32.
-
[13]
Kumar A, Schweizer HP. Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv Drug Deliv Rev 2005; 57: 1486–513.
-
[14]
Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Dev Biol 1992; 8: 67–113.
-
[15]
Fath MJ, Kolter R. ABC transporters: bacterial exporters. Microbiol Rev 1993; 57: 995–1017.
-
[16]
Kristiansen JE, Hendricks O, Delvin T, Butterworth TS, Aagaard L, Christensen JB, et al.. Reversal of resistance in microorganisms by help of non-antibiotics. J Antimicrob Chemother 2007; 59: 1217–79.
-
[17]
Levy SB. Active efflux mechanisms for antimicrobial resistance. Antimicrob Agents Chemother 1992; 36: 695.
-
[18]
Lewis K. In search of natural substrates and inhibitors of MDR pumps. J Mol Microbiol Biotechnol 2001; 3: 247–54.
-
[19]
Saier M. Jr, Tam R, Reizer A, Reizer J. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 1994; 11: 841–7.
-
[20]
Hürlimann LM, Corradi V, Hohl M, Bloemberg GV, Tieleman DP, Seeger MA. The heterodimeric ABC transporter EfrCD mediates multidrug efflux in Enterococcus faecalis. Antimicrob Agents Chemother 2016; 60: 5400–11.
-
[21]
Lerma LL, Benomar N, Valenzuela AS, Muñoz MdCC, Gálvez A, Abriouel H. Role of EfrAB efflux pump in biocide tolerance and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from traditional fermented foods and the effect of EDTA as EfrAB inhibitor. Food Microbiol 2014; 44: 249–57.
-
[22]
Levine DP. Vancomycin: a history. Clin Infect Dis 2006; 42: S5–12.
-
[23]
Gutiérrez-Castrellón P, Díaz-García L, de Colsa-Ranero A, Cuevas-Alpuche J, Jiménez-Escobar I. Efficacy and safety of ciprofloxacin treatment in urinary tract infections (UTIs) in adults: a systematic review with meta-analysis. Gac Med Mexico 2015; 151: 210–28.
-
[24]
Mandell L, Tillotson G. Safety of fluoroquinolones: an update. Can J Infect Dis Med 2002; 13: 54–61.
-
[25]
Huycke MM, Sahm DF, Gilmore MS. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis 1998; 4: 239.
-
[26]
Lee G. Ciprofloxacin resistance in Enterococcus faecalis strains isolated from male patients with complicated urinary tract infection. Korean J Urol 2013; 54: 388–93.
-
[27]
Matsumoto T, Hamasuna R, Ishikawa K, Takahashi S, Yasuda M, Hayami H, et al.. Nationwide survey of antibacterial activity against clinical isolates from urinary tract infections in Japan (2008). Int J Antimicrob Agents 2011; 37: 210–18.
-
[28]
Talebi M, Moghadam NA, Mamooii Z, Enayati M, Saifi M, Pourshafie MR. Antibiotic resistance and biofilm formation of Enterococcus faecalis in patient and environmental samples. Jundishapur J Microbiol 2015; 8: e23349.
-
[29]
Wayne P. CLSI. Performance standards for antimicrobial susceptibility testing; Twenty-fifth informational supplement. CLSI document M100-S25. Clinical and Laboratory Standards Institute; 2015.
-
[30]
Lerma LL, Benomar N, Valenzuela AS, Munoz MdCC, Gálvez A, Abriouel H. Role of EfrAB efflux pump in biocide tolerance and antibiotic resistance of Enterococcus faecalis and Enterococcus faecium isolated from traditional fermented foods and the effect of EDTA as EfrAB inhibitor. Food Microbiol 2014; 44: 249–57.
-
[31]
Shiadeh SMJ, Hashemi A, Fallah F, Lak P, Azimi L, Rashidan M. First detection of efrAB, an ABC multidrug efflux pump in Enterococcus faecalis in Tehran, Iran. Acta Microbiol Immunol Hung 2019; 66: 57–68.
-
[32]
Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, et al.. Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol 2006; 44: 2220–28.
-
[33]
Tendolkar PM, Baghdayan AS, Gilmore MS, Shankar N. Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect Immun 2004; 72: 6032–9.
-
[34]
Rutala WA, Kanamori H, Gergen MF, Knelson LP, Sickbert-Bennett EE, Chen LF, et al.. Enhanced disinfection leads to reduction of microbial contamination and a decrease in patient colonization and infection. Infect Cont Hosp Ep 2018; 39: 1118–21.
-
[35]
Levitus M, Perera TB. Vancomycin-Resistant Enterococci (Vre). StatPearls [Internet]. StatPearls Publishing; 2018.
-
[36]
Pazoles J, Talbot MK, Alder EA, White AC, Jonas BM, Murray BE, et al.. Enterococcus faecalis multi-drug resistance transporters: application for antibiotic discovery. J Mol Microbiol Biotechnol 2001; 3: 179–84.
-
[37]
Al-Jarousha A-MK, Saed A, Afifi H. Prevalence of multidrug resistant enterococci in nosocomial infection in Gaza strip. J Al-Aqsa Unv 2008; 12: 15–24.
-
[38]
Hasan AS, Nair D, Kaur J, Baweja G, Deb M, Aggarwal P. Resistance patterns of urinary isolates in a tertiary Indian hospital. J Ayub Med Coll Abbottabad 2007; 19: 39–41.
-
[39]
Kuch A, Willems RJ, Werner G, Coque TM, Hammerum AM, Sundsfjord A, et al.. Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J Antimicrob Chemother 2011; 67: 551–8.
-
[40]
Wang Q-Y, Li R-H, Shang X-H. Urinary tract infection caused by Enterococcus isolates: aetiology and antimicrobial resistance patterns. J Chemother 2015; 27: 117–19.
-
[41]
Yilema A, Moges F, Tadele S, Endris M, Kassu A, Abebe W, et al.. Isolation of enterococci, their antimicrobial susceptibility patterns and associated factors among patients attending at the University of Gondar Teaching Hospital. BMC Infect Dis 2017; 17: 276.
-
[42]
Lubelski J, Konings WN, Driessen AJ. Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria. Microbiol Mol Biol Rev 2007; 71: 463–76.
-
[43]
Kang S, Lee S, Choi S. Distribution of multidrug efflux pump genes in Enterococci spp. isolated from bovine milk samples and their antibiotic resistance patterns. Korean J Microbiol 2013; 49: 126–30.
-
[44]
Sanchez Valenzuela A, Lavilla Lerma L, Benomar N, Gálvez A, Perez Pulido R, Abriouel H. Phenotypic and molecular antibiotic resistance profile of Enterococcus faecalis and Enterococcus faecium isolated from different traditional fermented foods. Foodborne Pathog Dis 2013; 10: 143–9.
-
[45]
Mendes RE, Deshpande L, Streit JM, Sader HS, Castanheira M, Hogan PA, et al.. ZAAPS programme results for 2016: an activity and spectrum analysis of linezolid using clinical isolates from medical centres in 42 countries. J Antimicrob Chemother 2018; 73: 1880–7.
-
[46]
Said LB, Klibi N, Lozano C, Dziri R, Slama KB, Boudabous A, et al.. Diversity of enterococcal species and characterization of high-level aminoglycoside resistant enterococci of samples of wastewater and surface water in Tunisia. Sci Total Environ 2015; 530: 11–17.
-
[47]
Sassi M, Guérin F, Zouari A, Beyrouthy R, Auzou M, Fines-Guyon M, et al.. Emergence of optrA-mediated linezolid resistance in enterococci from France, 2006–16. J Antimicrob Chemother 2019; 74: 1469–72.
-
[48]
Zhou W, Gao S, Xu H, Zhang Z, Chen F, Shen H, et al.. Distribution of the optrA gene in Enterococcus isolates at a tertiary care hospital in China. J Glob Antimicrob Re 2019; 17: 180–6.
-
[49]
Chen H, Wang X, Yin Y, Li S, Zhang Y, Wang Q, et al.. Molecular characteristics of oxazolidinone resistance in enterococci from a multicenter study in China. BMC Med 2019; 19: 162.
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