First description of plasmid-mediated quinolone resistance determinants and β-lactamase encoding genes in non-typhoidal Salmonella isolated from humans, one companion animal and food in Romania

Gut Pathogens

Marian Mihaiu³  Simona Mirel²  Ovidiu Oniga²  Mirela Flonta¹  Alexandra Tabaran³  Liora Colobatiu² 

[1] Infectious Diseases Hospital, Cluj-Napoca, Romania;Faculty of Pharmacy, Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania;Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania

关键词: Public health;    Genetic relatedness;    Food;    Companion animal;    Humans;    Resistance mechanisms;    Antimicrobial resistance;    Salmonella;   

Others  :  1217974
DOI  :  10.1186/s13099-015-0063-3

 received in 2015-04-27, accepted in 2015-06-16,  发布年份 2015

【 摘 要 】

Background

Gastroenteritis attributable to Salmonella enterica and the continuous increase in antimicrobial resistance of this gut pathogen, which compromises the use of previously effective treatments, is of great concern for public health. This study was conducted in order to investigate the presence of plasmid-mediated quinolone resistance (PMQR) determinants and β-lactamase-encoding genes, in S. enterica, isolated from humans, one companion animal and food. Moreover, the study aimed to identify potential vehicles of transmission of resistant strains to humans, with focus on food products (meat).

Methods

A total of 20 S. enterica isolates recovered from food (chicken and pork meat), one companion animal and humans (stool samples), were examined for their serotype, antimicrobial susceptibility and the presence of PMQR and β-lactamase-encoding genes. Moreover, the genetic relatedness of nine Salmonella Infantis and ten Salmonella Enteritidis isolates was analyzed by pulsed-field gel electrophoresis (PFGE).

Results

Among all isolates, 15 (75%) were multidrug-resistant (MDR) and the majority of them proved to be resistant to nalidixic acid and fluoroquinolones (FQs) (ciprofloxacin and levofloxacin). Twelve isolates (60%) harboured at least one PMQR gene [qnrA, qnrB, qnrS, aac (6′)-Ib-cr or qepA] while seven isolates (35%) carried at least one β-lactamase-encoding gene (bla_TEM , bla_PSE-1 , bla_SHVor bla_CTX-M ). Moreover, two or more PMQR or β-lactamase-encoding genes co-existed in a single S. enterica isolate. A number of nine Salmonella Infantis, as well as the majority of Salmonella Enteritidis isolates analyzed by PFGE proved to be closely related.

Conclusions

The study demonstrated the co-existence of PMQR and β-lactamase-encoding genes among the Salmonella isolates recovered and confirmed that multiple mechanisms might be involved in the acquisition and spread of resistance determinants. The close genetic relatedness between the clinical and foodborne S. enterica isolates, suggested that chicken meat might be a possible cause of human salmonellosis in our country, during the study period. Results of this study might improve understanding of the antimicrobial resistance mechanisms and transmission dynamics of Salmonella spp. Here, we report for the first time the presence of PMQR and β-lactamase-encoding genes in S. enterica isolates, recovered from humans, one companion animal and food, in Romania.

【 授权许可】

   
2015 Colobatiu et al.

【 图 表 】

Figure1.

Figure2.

【 参考文献 】

• [1]Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DMA, Jensen AB, Wegener HC et al.. Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis. 2011; 8(8):887-900.
• [2]Swaminathan B, Gerner-Smidt P, Barrett T. Focus on Salmonella. Foodborne Pathog Dis. 2006; 3(2):154-156.
• [3]The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. 2015; 13(1):3991.
• [4]Cui S, Li J, Sun Z, Hu C, Jin S, Li F et al.. Characterization of Salmonella enterica isolates from infants and toddlers in Wuhan, China. J Antimicrob Chemother. 2009; 63(1):87-94.
• [5]Mihaiu L, Lapusan A, Tanasuica R, Sobolu R, Mihaiu R, Oniga O et al.. First study of Salmonella in meat in Romania. J Infect Dev Ctries. 2014; 8:50-58.
• [6]Clemente L, Manageiro V, Ferreira E, Jones-Dias D, Correia I, Themudo P et al.. Occurrence of extended-spectrum β-lactamases among isolates of Salmonella enterica subsp. enterica from food-producing animals and food products, in Portugal. Int J Food Microbiol. 2013; 167(2):221-228.
• [7]Dionisi AM, Lucarelli C, Benedetti I, Owczarek S, Luzzi I. Molecular characterisation of multidrug-resistant Salmonella enterica serotype Infantis from humans, animals and the environment in Italy. Int J Antimicrob Agents. 2011; 38(5):384-389.
• [8]Kozoderović G, Velhner M, Jelesić Z, Golić N, Lozo J, Kehrenberg C. Prevalence of quinolone resistance and mutations in the topoisomerase genes in Salmonella enterica serotype Enteritidis isolates from Serbia. Int J Antimicrob Agents. 2012; 40:455-457.
• [9]Jiang HX, Song L, Liu J, Zhang XH, Ren YN, Zhang WH et al.. Multiple transmissible genes encoding fluoroquinolone and third-generation cephalosporin resistance co-located in non-typhoidal Salmonella isolated from food-producing animals in China. Int J Antimicrob Agents. 2014; 43(3):242-247.
• [10]Wang Y, Yang B, Wu Y, Zhang Z, Meng X, Xi M et al.. Molecular characterization of Salmonella enterica serovar Enteritidis on retail raw poultry in six provinces and two National cities in China. Food Microbiol. 2015; 46:74-80.
• [11]Wasyl D, Hoszowski A, Zajac M. Prevalence and characterisation of quinolone resistance mechanisms in Salmonella spp. Vet Microbiol. 2014; 171:307-314.
• [12]Toboldt A, Tietze E, Helmuth R, Junker E, Fruth A, Malorny B. Molecular epidemiology of Salmonella enterica serovar Kottbus isolated in Germany from humans, food and animals. Vet Microbiol. 2014; 170(1–2):97-108.
• [13]Dan SD, Tabaran A, Mihaiu L, Mihaiu M. Antibiotic susceptibility and prevalence of foodborne pathogens in poultry meat in Romania. J Infect Dev Ctries. 2015; 9(1):35-41.
• [14]Afema JA, Mather AE, Sischo WM. Antimicrobial resistance profiles and diversity in Salmonella from humans and cattle, 2004–2011. Zoonoses Public Health. 2014.
• [15]Lunguya O, Lejon V, Phoba M-F, Bertrand S, Vanhoof R, Glupczynski Y et al.. Antimicrobial resistance in invasive non-typhoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLoS Negl Trop Dis. 2013; 7(3):e2103.
• [16]Critically important antimicrobials for human medicine, 3rd revision. World Health Organization, Geneva; 2011.
• [17]Arlet G, Barrett TJ, Butaye P, Cloeckaert A, Mulvey MR, White DG. Salmonella resistant to extended-spectrum cephalosporins: prevalence and epidemiology. Microbes Infect. 2006; 8(7):1945-1954.
• [18]Ruiz J, Pons MJ, Gomes C. Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents. 2012; 40:196-203.
• [19]Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A et al.. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother. 2006; 50(4):1178-1182.
• [20]Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S et al.. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother. 2009; 53(5):1892-1897.
• [21]Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother. 2006; 50(8):2872-2874.
• [22]Poirel L, Cattoir V, Nordmann P. Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbiol. 2012; 3:24.
• [23]Verraes C, Van Boxstael S, Van Meervenne E, Van Coillie E, Butaye P, Catry B et al.. Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health. 2013; 10(7):2643-2669.
• [24]Angulo FJ, Nargund VN, Chiller TC. Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. J Vet Med B Infect Dis Vet Public Health. 2004; 51(8–9):374-379.
• [25]Antibiotics curently in clinical development [Internet]. Available from:. http://www. pewtrusts.org/en/multimedia/data-visualizations/2014/antibiotics-currently-in-clinical-development webcite
• [26]Barua H, Biswas PK, Talukder KA, Olsen KEP, Christensen JP. Poultry as a possible source of non-typhoidal Salmonella enterica serovars in humans in bangladesh. Vet Microbiol. 2014; 168(2–4):372-380.
• [27]Threlfall EJ, Ward LR, Rowe B. Resistance to ciprofioxacin in non-typhoidal Salmonellas from humans in England and Wales—the current situation. Clin Microbiol Infect. 1999; 5(3):130-134.
• [28]Scientific of EFSA and ECDC:the European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J. 2012; 10(3):2597.
• [29]Veldman K, Cavaco LM, Mevius D, Battisti A, Franco A, Botteldoorn N et al.. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother. 2011; 66:1278-1286.
• [30]Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev. 2009; 22(4):664-689.
• [31]Kim KY, Park JH, Kwak HS, Woo GJ. Characterization of the quinolone resistance mechanism in foodborne Salmonella isolates with high nalidixic acid resistance. Int J Food Microbiol. 2011; 146(1):52-56.
• [32]Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet. 1998; 351(9105):797-799.
• [33]Briales A, Rodríguez-Martínez JM, Velasco C, Díaz de Alba P, Domínguez-Herrera J, Pachón J et al.. In vitro effect of qnrA1, qnrB1, and qnrS1 genes on fluoroquinolone activity against isogenic Escherichia coli isolates with mutations in gyrA and parC. Antimicrob Agents Chemother. 2011; 55(3):1266-1269.
• [34]Ruiz J, Pons MJ, Gomes C. Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents. 2012; 40(3):196-203.
• [35]Robicsek A, Strahilevitz J, Sahm DF, Jacoby G, Hooper DC. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother. 2006; 50(8):2872-2874.
• [36]D’Andrea MM, Arena F, Pallecchi L, Rossolini GM. CTX-M-type β-lactamases: a successful story of antibiotic resistance. Int J Med Microbiol. 2013; 303(6–7):305-317.
• [37]Yang T, Zeng Z, Rao L, Chen X, He D, Lv L et al.. The association between occurrence of plasmid-mediated quinolone resistance and ciprofloxacin resistance in Escherichia coli isolates of different origins. Vet Microbiol. 2014; 170(1–2):89-96.
• [38]Vien LTM, Minh NNQ, Thuong TC, Khuong HD, Nga TVT, Thompson C et al.. The co-selection of fluoroquinolone resistance genes in the gut flora of Vietnamese children. PLoS One. 2012; 7(8):e42919.
• [39]Yang B, Wang Q, Cui S, Wang Y, Shi C, Xia X et al.. Characterization of extended-spectrum beta-lactamases-producing Salmonella strains isolated from retail foods in Shaanxi and Henan Province, China. Food Microbiol. 2014; 42:14-18.
• [40]WHO (2007) Critically important antimicrobials for human medicine: categorization for the development of risk management strategies to contain antimicrobial resistance due to non human antimicrobial use: report of the second WHO Expert Meeting, 29–31 May 2007, Copenhagen
• [41]Van TTH, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol. 2008; 124(3):217-223.
• [42]Simjee S, White DG, McDermott PF, Wagner DD, Zervos MJ, Donabedian SM et al.. Characterization of Tn1546 in vancomycin-resistant Enterococcus faecium isolated from canine urinary tract infections: evidence of gene exchange between human and animal Enterococci. J Clin Microbiol. 2002; 40(12):4659-4665.
• [43]Guardabassi L, Schwarz S, Lloyd DH. Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother. 2004; 54(2):321-332.
• [44]Clinical and Laboratory Standards Institute (2013) M100-S23 performance standards for antimicrobial susceptibility testing; twenty-third informational supplement, pp 44–49
• [45]Randall LP, Cooles SW, Osborn MK, Piddock LJV, Woodward MJ. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J Antimicrob Chemother. 2004; 53(2):208-216.
• [46]Carlson SA, Bolton LF, Briggs CE, Hurd HS, Sharma VK, Fedorka-Cray PJ et al.. Detection of multiresistant Salmonella typhimurium DT104 using multiplex and fluorogenic PCR. Mol Cell Probes. 1999; 13(3):213-222.
• [47]Gallardo F, Ruiz J, Marco F, Towner KJ, Vila J. Increase in incidence of resistance to ampicillin, chloramphenicol and trimethoprim in clinical isolates of Salmonella serotype Typhimurium with investigation of molecular epidemiology and mechanisms of resistance. J Med Microbiol. 1999; 48(4):367-374.
• [48]Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. beta-Lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother. 2005; 56(1):115-121.
• [49]Weill F-X, Guesnier F, Guibert V, Timinouni M, Demartin M, Polomack L et al.. Multidrug resistance in Salmonella enterica serotype Typhimurium from humans in France (1993 to 2003). J Clin Microbiol. 2006; 44(3):700-708.
• [50]Lunn AD, Fàbrega A, Sánchez-Céspedes J, Vila J. Prevalence of mechanisms decreasing quinolone-susceptibility among Salmonella spp. clinical isolates. Int Microbiol. 2010; 13:15-20.
• [51]Cattoir V, Weill F-X, Poirel L, Fabre L, Soussy C-J, Nordmann P. Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother. 2007; 59(4):751-754.
• [52]Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B et al.. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis. 2006; 3(1):59-67.
• [53]Usein C-R, Străuţ M, Palade A-M, Tatu-Chiţoiu D, Ciontea SA, Băltoiu MC et al.. A multiple typing approach is recommended for the laboratory-based surveillance of salmonellosis in Romania. Roum Arch Microbiol Immunol. 2010; 69(4):197-203.
• [54]Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH et al.. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995; 33(9):2233-2239.