Iranian Journal of Microbiology 2017. 9(2):74-81.

Phenotypic and genetic characterization of β-lactam resistance in Klebsiella from retail chicken meat in Mansoura, Egypt
Hazem Ramadan, Amal Awad


Background and Objectives: This study was undertaken to characterize antimicrobial resistance phenotypes and genes encoding extended spectrum β-lactamases (ESBLs) in Klebsiella isolated from retail chicken meat in Mansoura, Egypt.
Materials and Methods: Three hundred sixty chicken meat samples from 120 eviscerated chicken carcasses (3 cuts each) collected randomly from local retail chicken shops in Mansoura, Egypt during the period from April to June 2015, were assayed for the presence of Klebsiella by conventional bacteriological methods. Antimicrobial sensitivity for 12 antimicrobials using disk diffusion, ESBL phenotypic confirmation and PCR characterization of ESBL-encoding genes (blaTEM, blaCTX-M, blaOXA, blaSHV and blaCMY) were performed.
Results: Klebsiella was identified from 22.2% (80/360) of the samples. Of the 12 antimicrobials tested, multidrug resistance (MDR; resistance to ≥3 of the antimicrobial classes) was observed in 96.25% (77/80) of the Klebsiella isolates. All the isolates were resistant to cefotaxime, ceftriaxone and aztreonam. ESBL-producers were phenotypically confirmed in 48.75% (39/80) of the isolates. The highest values (0.75 and 0.67) of multiple antibiotic resistance (MAR) significantly occurred in ESBL-producing isolates. PCR findings showed a significantly higher occurrence of β-lactamase encoding genes in ESBL (94.9%, 37/39) than non-ESBL producing isolates (4.9%, 2/41). The distribution of blaTEM, blaCTX-M and blaOXA among ESBL-producing isolates was 84.6%, 30.8% and 25.6%, respectively.
Conclusion: Efficient monitoring and tracking of MDR, especially β-lactam resistance, in food sources is essential to predict the potential hazards for human infections.


Klebsiella; Retail chicken meat; Antimicrobial resistance; ESBL; Food-borne pathogens

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Frye JG, Jackson CR. Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from U.S. food animals. Front Microbiol 2013; 4:135.

Karlowsky JA, Jones ME, Thornsberry C, Friedland IR, Sahm DF. Trends in antimicrobial susceptibilities among Enterobacteriaceae isolated from hospitalized patients in the United States from 1998 to 2001. Antimicrob Agents Chemother 2003; 47:1672-1680.

Davis GS, Price LB. Recent research examining links among Klebsiella pneumoniae from food, food animals, and human extraintestinal infections. Curr Environ Health Rep 2016; 3:128-135.

Struve C, Krogfelt KA. Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ Microbiol 2004; 6:584-590.

Kim SH, Wei CI, Tzou YM, An H. Multidrug-Resistant Klebsiella pneumoniae isolated from farm environments and retail products in Oklahoma. J Food Prot 2005; 68:2022-2029.

Price LB, Graham JP, Lackey LG, Roess A, Vailes R, Silbergeld E. Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environ Health Perspect 2007;115:1738-1742.

Calbo E, Freixas N, Xercavins M, Riera M, Nicolás C, Monistrol O, et al. Foodborne nosocomial outbreak of SHV1 and CTX-M-15-producing Klebsiella pneumoniae: epidemiology and control. Clin Infect Dis 2011; 52:743-749.

Davis GS, Waits K, Nordstrom L, Weaver B, Aziz M, Gauld L, et al. Intermingled Klebsiella pneumoniae populations between retail meats and human urinary tract infections. Clin Infect Dis 2015; 61:892-899.

Guo Y, Zhou H, Qin L, Pang Z, Qin T, Ren H, et al. Frequency, antimicrobial resistance and genetic diversity of Klebsiella pneumoniae in food samples. PLoS One 2016; 11(4): e0153561.

Rasschaert G, Houf K, De Zutter L. Impact of

slaughter line contamination on the presence of Salmonella on broiler carcasses. J Appl Microbiol 2007; 103:333-341.

Paterson DL, Bonomo RA. Extended-spectrum ß-lactamases: A clinical update. Clin Microbiol Rev 2005; 18: 657-686.

Falagas ME, Karageorgopoulos DE. Extended-spectrum beta-lactamase-producing organisms. J Hosp Infect 2009; 73:345-354.

Su LH, Chu C, Cloeckaert A, Chiu CH. An epidemic of plasmids? Dissemination of extended-spectrum cephalosporinases among Salmonella and other Enterobacteriaceae. FEMS Immunol Med Microbiol 2008; 52:155-168.

Cogliani C, Goossens H, Greko C. Restricting antimicrobial use in food animals: a lesson from Europe. Microbe 2011; 6:274-279.

Dahshan H, Abd-Elall AM, Megahed AM, Abd-El-Kader MA, Nabawy EE. Veterinary antibiotic resistance, residues, and ecological risks in environmental samples obtained from poultry farms, Egypt. Environ Monit Assess 2015; 187:1-10.

Collee JG, Miles RS, Watt B (1996). Tests for identification of bacteria. In: Collee JG, Fraser AG, Marmion BP, Simmons A (Eds): Mackie and McCartney Practical Medical Microbiology, 14th ed. Churchill Livingstone, New York, pp. 131-151.

Hansen DS, Aucken HM, Abiola T, Podschun R. Recommended test panel for differentiation of Klebsiella species on the basis of a trilateral inter-laboratory evaluation of 18 biochemical tests. J Clin Microbiol 2004; 42:3665-3669.

Clinical and Laboratory Standards Institute (CLSI) 2011. M100-S21. Vol. 31 No. 1.

Krumperman PH. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 1983; 46:165-170.

Ramadan H, Awad A, Ateya A. Detection of phenotypes, virulence genes and phylotypes of avian pathogenic and human diarrheagenic Escherichia coli in Egypt. J Infect Dev Ctries 2016; 10:584-591.

Zhao S, QaiyumiS, Friedman S, Singh R, Foley SL, White DG, et al. Characterization of Salmonella enterica serotype Newport isolated from humans and food animals. J Clin Microbiol 2003; 41:5366-5371.

Ahmed AM, Furuta K, Shimomura K, Kasama Y, Shimamoto T. Genetic characterization of multidrug resistance in Shigella spp. from Japan. J Med Microbiol 2006; 55:1685-1691.

Weill FX, Demartin M, Tandé D, Espié E, Rakotoarivony I, Grimont PAD. SHV-12-like extended-spectrum-beta-lactamase-producing strains of Salmonella enterica serotypes Babelsberg and Enteritidis isolated in France among infants adopted from Mali. J Clin Microbiol 2004; 42:2432-2437.

Siu LK, Lo JY, Yuen KY, Chau PY, Ng MH, Ho PL. β-Lactamases in Shigella flexneri isolates from Hong Kong and Shanghai and a novel OXA-1-like β-lactamase, OXA-30. Antimicrob Agents Chemother 2000; 44:2034-2038.

Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, et al. Zoo animals as reservoirs of Gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol 2007; 73:6686-6690.

Kilonzo-Nthenge A, Nahashon SN, Chen F, Adefope N. Prevalence and antimicrobial resistance of pathogenic bacteria in chicken and guinea fowl. Poult Sci 2008; 87:1841-1848.

Gundogan N, Avci E. Prevalence and antibiotic resistance of extended spectrum beta-lactamase (ESBL) producing Escherichia coli and Klebsiella species isolated from foods ofanimal origin in Turkey. Afr J Microbiol Res 2013; 7:4059-4064.

Kilonzo-Nthenge A, Rotich E, Nahashon SN. Evaluation of drug-resistant Enterobacteriaceae in retail poultry and beef. Poult Sci 2013; 92:1098-1107.

Wu H, Liu BG, Liu JH, Pan YS, Yuan L, Hu GZ. Phenotypic and molecular characterization of CTX-M-14 extended-spectrum β-lactamase and plasmid-mediated ACT-like AmpC β-lactamase produced by Klebsiella pneumoniae isolates from chickens in Henan Province, China. Genet Mol Res 2012; 11: 3357-3364.

Ullah F, Malik SA, Ahmed J. Antimicrobial susceptibility pattern and ESBL prevalence in Klebsiella pneumoniae from urinary tract infections in the North-West of Pakistan. Afr J Microbiol Res 2009; 3:676-680.

Gundogan N, Citak S, Yalcin E. Virulence properties of extended spectrum β-lactamase-producing Klebsiella species in meat samples. J Food Prot 2011; 74:559-564.

Livermore DM. Beta-lactamases in laboratory and clinical resistance. Clin Microbiol Rev 1995;8:557-584.

Ahmed AM, Shimamoto T. Genetic analysis of multiple antimicrobial resistance in Salmonella isolated from diseased broilers in Egypt. Microbiol Immunol 2012; 56:254-261.

Halawa M, Moawad A, Eldesouky I, Ramadan H. Detection of Antimicrobial phenotypes, β-Lactamase encoding genes and class I integrons in Salmonella serovars isolated from broilers. Int J Poult Sci 2016; 15: 1-7.

Ahmed AM, Shimamoto T, Shimamoto T. Molecular characterization of multidrug-resistant avian pathogenic Escherichia coli isolated from septicemic broilers. Int J Med Microbiol 2013; 303:475-483.

Wu H, Wang M, Liu Y, Wang X, Wang Y, Lu J, et al. Characterization of antimicrobial resistance in Klebsiella species isolated from chicken broilers. Int J Food Microbiol 2016; 232:95-102.

Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis 2011; 17:1216-1222.

Overdevest IT, Heck M, van der Zwaluw K, Huijsdens X, van Santen M, Rijnsburger M, et al. Extended-spectrum β-lactamase producing Klebsiella spp. in chicken meat and humans: a comparison of typing methods. Clin Microbiol Infect 2014; 20: 251-255.

Casella T, Rodríguez MM, Takahashi JT, Ghiglione B, Dropa M, Assunção E, et al. Detection of blaCTX-M-type genes in complex class 1 integrons carried by Enterobacteriaceae isolated from retail chicken meat in Brazil. Int J Food Microbiol 2015; 197:88-91.

Tekiner İH, Özpınar H. Occurrence and characteristics of extended spectrum β-lactamases-producing Enterobacteriaceae from foods of animal origin. Braz J Microbiol 2016; 47: 444-451.

Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs 2003; 63:353-365.

Haque A, Yoshizumi A, Saga T, Ishii Y, Tateda K. ESBL-producing Enterobacteriaceae in environmental water in Dhaka, Bangladesh. J Infect Chemother 2014; 20:735-737.


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