Open Access
Research (Published online: 12-04-2018)
10. Characterization of quinolone-resistant Enterobacteriaceae strains isolated from poultry in Western Algeria: First report of qnrS in an Enterobacter cloacae
Qada Benameur, Hassiba Tali-Maamar, Farida Assaous, Badia Guettou, Meki Boutaiba Benklaouz, Kheira Rahal and Meriem-Hind Ben-Mahdi
Veterinary World, 11(4): 469-473

Qada Benameur: Faculty of Natural Sciences and Life, Abdelhamid Ibn Badis University, Mostaganem, Algeria; Research Laboratory, Health and Animal Production, Higher National Veterinary School, Algiers, Algeria.
Hassiba Tali-Maamar: Medical Bacteriology Laboratory, Pasteur Institute of Algeria, Algiers, Algeria.
Farida Assaous: Medical Bacteriology Laboratory, Pasteur Institute of Algeria, Algiers, Algeria.
Badia Guettou: Medical Bacteriology Laboratory, Pasteur Institute of Algeria, Algiers, Algeria.
Meki Boutaiba Benklaouz: Veterinary Sciences Institute, Ibn Khaldoun University, Tiaret, Algeria.
Kheira Rahal: Medical Bacteriology Laboratory, Pasteur Institute of Algeria, Algiers, Algeria.
Meriem-Hind Ben-Mahdi: Research Laboratory, Health and Animal Production, Higher National Veterinary School, Algiers, Algeria; Higher School of Food Sciences and Agro-alimentary Industries, Algiers, Algeria.

doi: 10.14202/vetworld.2018.469-473

Share this article on [Facebook] [LinkedIn]

Article history: Received: 21-12-2017, Accepted: 06-03-2018, Published online: 12-04-2018

Corresponding author: Qada Benameur


Citation: Benameur Q, Tali-Maamar H, Assaous F, Guettou B, Boutaiba Benklaouz M, Rahal K, Ben-Mahdi MH (2018) Characterization of quinolone-resistant Enterobacteriaceae strains isolated from poultry in Western Algeria: First report of qnrS in an Enterobacter cloacae, Veterinary World, 11(4): 469-473.

Aim: Multidrug-resistant (MDR) Enterobacteriaceae have frequently been reported, in both human and veterinary medicine, from different parts of the world as a consequence of antibiotic usage. However, there is a lack of published data regarding antimicrobial resistance in non-Escherichia coli (E. coli) Enterobacteriaceae from animals in Algeria. This study aimed to evaluate the frequency of resistance to antibiotics with a focus on quinolones and to investigate the presence of qnr genes in Enterobacteriaceae of poultry origin.

Materials and Methods: A total of 310 samples of poultry origin were collected from 2010 to 2014 from broiler and layer farms and hatcheries located in different geographic areas of Western Algeria (including Mostaganem, Oran, Mascara, Relizane, Chlef, Tiaret, and Tissemsilt). Antimicrobial susceptibility testing was performed using disc diffusion assay. Polymerase chain reaction and sequencing accomplished the characterization of qnr genes (qnrA, qnrB, and qnrS).

Results: A total of 253 Enterobacteriaceae strains were isolated in this study. These isolates exhibited high levels of resistance to quinolones and other families of antibiotics. All the strains isolated in this study were resistant to at least one antibiotic. Among them, 233 (92.09%) were considered MDR. Among the 18 randomly selected nalidixic acid (NA)- resistant Enterobacteriaceae isolates, one E. coli and one Enterobacter cloacae were carrying qnrS1. By contrast, qnrA and qnrB were not detected in this study.

Conclusion: This is the first report on the identification of the qnrS gene in E. cloacae isolated from animal source in Algeria. Further studies have to be conducted to determine the real prevalence of qnr genes.

Keywords: Algeria, antimicrobial resistance, Enterobacteriaceae, qnrS1.


1. Richter, S.N., Frasson, I., Bergo, C., Manganelli, R., Cavallaro, A. and Palu, G. (2010) Characterisation of qnr plasmid-mediated quinolone resistance in Enterobacteriaceae from Italy: Association of the qnrB19 allele with the integron element ISCR1 in Escherichia coli. Int. J. Antimicrob. Agents., 35: 578-583. [Crossref]

2. Robicsek, A., Jacoby, G.A. and Hooper, D.C. (2006) The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis., 6: 629-640. [Crossref]

3. Yadav, K.K., Adhikari, N., Khadka, R., Pant, A.D. and Shah, B. (2015) Multidrug-resistant Enterobacteriaceae and extended spectrum β-lactamase producing Escherichia coli: A cross-sectional study in national kidney center, Nepal. Antimicrob. Resist. Infect. Control., 4: 42. [Crossref] [PubMed] [PMC]

4. Kilonzo-Nthenge, A., Rotich, E. and Nahashon, S.N. (2013) Evaluation of drug-resistant Enterobacteriaceae in retail poultry and beef. Poult. Sci., 92: 1098-1107. [Crossref] [PubMed]

5. Benameur, Q., Guemour, D., Hammoudi, A., Aoudia, K., Aggad, H., Humblet, M.H. and Saegermang, C. (2014) Antimicrobial resistance of Escherichia coli isolated from chickens in West of Algeria. Int. J. Sci. Basic Appl. Res., 13: 366-370.

6. Hammoudi, A. and Aggad, H. (2008) Antibioresistance of Escherichia coli strains isolated from chicken colibacillosis in Western Algeria. Turk. J. Vet. Anim. Sci., 32: 123-126.

7. Aggad, H., Ammar, Y.A., Hammoudi, A. and Kihal, M. (2010), Antimicrobial resistance of Escherichia coli isolated from chickens with colibacillosis. Glob. Vet., 4: 303-306.

8. Benameur, Q., Ben-Mahdi, M.H., Boutaiba Benklaouz, M., Tali-Maamar, H., Assaous, F., Guettou, B. and Rahal, K. (2016) Analysis of high levels of multidrug-resistant Escherichia coli from healthy broiler chickens in Western Algeria. Afr. J. Microbiol. Res., 10: 1792-1797. [Crossref]

9. Tran, J.H. and Jacoby, G.A. (2002) Mechanism of plasmid-mediated quinolone resistance. Proc. Natl. Acad. Sci. USA, 99: 5638-5642. [Crossref] [PubMed] [PMC]

10. Tran, J.H., Jacoby, G.A. and Hooper, D.C. (2005) Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV. Antimicrob. Agents. Chemother., 49: 3050-3052. [Crossref] [PubMed] [PMC]

11. Strahilevitz, J., Jacoby, G.A., Hooper, D.C. and Robicsek, A. (2009) Plasmid-mediated quinolone resistance: A multifaceted threat. Clin. Microbiol. Rev., 22: 664-689. [Crossref] [PubMed] [PMC]

12. Cattoir, V., Poirel, L. and Nordmann, P. (2007) Plasmid-mediated quinolone resistance determinant QnrB4 identified in France in an Enterobacter cloacae clinical isolate coexpressing a QnrS1 determinant. Antimicrob. Agents. Chemother., 51: 2652-2653. [Crossref] [PubMed] [PMC]

13. Cambau, E., Lascols, C., Sougakoff, V., Bebear, C., Bonnet, R., Cavallo, J.D., Gutmann, L., Ploy, M.C., Jarlier, V., Soussy, C.J. and Robert, J. (2006) Occurrence of qnrA-positive clinical isolates in French teaching hospitals during 2002-2005. Clin. Microbiol. Infect., 12: 1013-1020. [Crossref] [PubMed]

14. Iabadene, H., Messai, Y., Ammari, H., Ramdani-Bouguessa, N., Lounes, S., Bakour, R. and Arlet, G. (2008) Dissemination of ESBL and Qnr determinants in Enterobacter cloacae in Algeria. J. Antimicrob. Chemother., 62: 133-136. [Crossref] [PubMed]

15. Meradi, L., Djahoudi, A., Abdi, A., Bouchakour, M., Claude, J.D. and Timinouni, M. (2011) Qnr and Aac(6')-Ib-cr types quinolone resistance among Enterobacteriaceae isolated in Annaba, Algeria. Pathol. Biol., 59: 73-78. [Crossref] [PubMed]

16. Gharout-Sait, A., Touati, A., Benallaoua, S., Guillard, T., Brasm, T.J. and de Champs, C. (2012) CTX-M from community acquired urinary tract infections in Algeria. Afr. J. Microbiol. Res., 6: 5306-5313.

17. Clinical and Laboratory Standards Institute. (2015) Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fifth Informational Supplement document M100S25. Wayne, PA: Clinical and Laboratory Standards Institute.

18. Jacoby, G.A., Chow, N. and Waites, K.B. (2003), Prevalence of plasmid-mediated quinolone resistance. Antimicrob. Agents. Chemother., 47: 559-562. [Crossref] [PubMed] [PMC]

19. Jacoby, G.A., Walsh, K.E., Mills, D.M., Walker, V.J., Oh, H., Robicsek, A. and Hooper, D.C. (2006) qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob. Agents. Chemother., 50: 1178-1182. [Crossref] [PubMed] [PMC]

20. Gay, K., Robicsek, A., Strahilevitz, J., Park, C.H., Jacoby, G., Barrett, T.J., Medalla, F., Chiller, T.M. and Hooper, D.C. (2006) Plasmid-mediated quinolone resistance in non-typhi serotypes of Salmonella enterica. Clin. Infect. Dis., 43: 297-304. [Crossref] [PubMed]

21. Ling, T.X., Xiong, J., Yu, Y., Lee, C.C., Ye, H. and Hawkey, P.M. (2006) Multicenter antimicrobial susceptibility survey of gram-negative bacteria isolated from patients with community-acquired infections in the people's republic of China. Antimicrob. Agents. Chemother., 50: 374-378. [Crossref]

22. Silva-Sanchez, J., Barrios, H., Reyna-Flores, F., Bello-Diaz, M., Sanchez-Perez, A., Rojas, T., Bacterial Resistance Consortium and Garza-Ramos, U. (2011) Prevalence and characterization of plasmid-mediated quinolone resistance genes in extended-spectrum β-lactamase-producing Enterobacteriaceae isolates in Mexico. Microb. Drug. Resist., 17: 497-505. [Crossref] [PubMed]

23. Belmahdi, M., Bakour, S., Al Bayssari, C., Touati, A. and Rolain, J.M. (2016) Molecular characterization of extended-spectrum β-lactamase- and plasmid AmpC-producing Escherichia coli strains isolated from broilers in Bejala, Algeria. J. Glob. Antimicrob. Resist., 6: 108-112. [Crossref] [PubMed]

24. Yousfi, M., Mairi, A., Touati, A., Hassissene, L., Brasme, L., Guillard, T. and De Champs, C. (2016) Extended spectrum β-lactamase and plasmid-mediated quinolone resistance in Escherichia coli fecal isolates from healthy companion animals in Algeria. J. Infect. Chemother., 22: 431-435. [Crossref]

25. Cavaco, L.M., Hendriksen, R.S. and Aarestrup, F.M. (2007) Plasmid-mediated quinolone resistance determinant qnrS1 detected in Salmonella enterica serovar Corvallis strains isolated in Denmark and Thailand. J. Antimicrob. Chemother., 60: 704-706. [Crossref] [PubMed]

26. Ferrari, R., Galiana, A., Cremades, R., Rodriguez, J.C., Magnani, M., Tognim, M.C.B., Oliveira, T.C.R.M. and Royo, G. (2011) Plasmid-mediated quinolone resistance by genes qnrA1 and qnrB19 in Salmonella strains isolated in Brazil. J. infect. Dev. Ctries, 5: 496-498. [Crossref] [PubMed]

27. Veldman, K., van Pelt, W. and Mevius, D. (2008) First report of qnr genes in Salmonella in the Netherlands. J. Antimicrob. Chemother., 61: 452-453. [Crossref] [PubMed]

28. Fortini, D., Fashae, K., Garcia-Fernandez, A., Villa, L. and Carattoli, A. (2011) Plasmid-mediated quinolone resistance and beta-lactamases in Escherichia coli from healthy animals from Nigeria. J. Antimicrob. Chemother., 66: 1269-1272. [Crossref] [PubMed]

29. Ma, J., Zeng, Z., Chen, Z., Xu, X., Wang, X., Deng, Y., Lue, D., Huang, L., Zhang, Y., Liu, L. and Wang, M. (2009) High prevalence of plasmid-mediated quinolone resistance determinants qnr, aac(6')-Ib-cr, and qepA among ceftiofur-resistant Enterobacteriaceae isolates from companion and food-producing animals. Antimicrob. Agents. Chemother., 53: 519-524. [Crossref]

30. Kirchner, M., Wearing, H. and Teale, C. (2011) Plasmid-mediated quinolone resistance gene detected in Escherichia coli from cattle. Vet. Microbiol., 148: 434-435. [Crossref] [PubMed]

31. Poirel, L., Leviandier, C. and Nordmann, P. (2006) Prevalence and genetic analysis of plasmid-mediated quinolone resistance determinants QnrA and QnrS in Enterobacteriaceae isolates from a French university hospital. Antimicrob. Agents. Chemother., 50: 3992-3997. [Crossref]

32. Robicsek, A., Strahilevitz, J., Sahm, D.F., Jacoby, G.A. and Hooper, D.C. (2006) Qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob. Agents. Chemother., 50: 2872-2874. [Crossref] [PubMed] [PMC]

33. Martinez-Martinez, L., Cano, M.E., Rodriguez-Martinez, J.M., Calvo, J. and Pascual, A. (2008) Plasmid-mediated quinolone resistance. Expert. Rev. Anti. Infect. Ther., 6: 685-711. [Crossref] [PubMed]

34. Martinez-Martinez, L., Pascual, A. and Jacoby, G.A. (1998) Quinolone resistance from a transferable plasmid. Lancet, 351: 797-799. [Crossref]

35. Johnson, J.R., Kuskowski, M.A., Menard, M., Gajewski, A., Xercavins, M. and Garau, J. (2006) Similarity between human and chicken Escherichia coli isolates in relation to ciprofloxacin resistance status. J. Infect. Dis., 194: 71-78. [Crossref] [PubMed]

36. Agabou, A., Lezzar, N., Ouchenane, Z., Khemissi, S., Satta, D., Sotto, A., Lavigne, J.P. and Pantel, A. (2015) Clonal relationship between human and avian ciprofloxacin-resistant Escherichia coli isolates in North-Eastern Algeria. Eur. J. Clin. Microbiol. Infect. Dis., 35: 227-234. [Crossref] [PubMed]