Genetic heterogeneity of CTX-M type extended-spectrum ß-lactamase producing Escherichia coli strains from diverse sources in Saudi Arabia

Authors

  • Sabry A Hassan Taif University, Saudi Arabia South Valley University, Egypt
  • Youssuf A. Gherbawy
  • Abdallah D. Altalhi

DOI:

https://doi.org/10.3823/768

Keywords:

Molecular typing, E. coli, CTX-M type ESBLs, RAPD-PCR

Abstract

Background: The rise of CTX-M extended spectrum β-lactamase (ESBLs)-producing E. coli in non-human sources is a growing concern of public health. Understanding the extent of public health risk attributed to CTX-M type ESBLs-producing strains from different sources is critical for effective control.

Objective: This study focuses on detection and molecular typing of CTX-M type ESBL-producing E. coli isolated from various sources in Taif, Western Saudi Arabia. 

Material and Methods: A total of 24 E. coli ESBLs-producing isolates from multiple sources were assessed for the presence of CTX-M groups gene by PCR, and subsequently their clonal relatedness by random amplifid of polymorphic DNA (RAPD) analysis. Isolates were selected according to a resistance phenotype consistent with production of ESBL-type beta-lactamase using double disk diffusion method.

Results: A CTX-M gene was detected in all 24 isolates. RAPD typing of E. coli isolates bearing CTX-M gene showed 24 patterns verifid into two major clusters (A, B) and three sub-clusters (A1 – A3). Phylogenetic analysis indicating a degree of similarity among clustering isolates from human, sheep and raw milk origins. Identical profie was observed between three isolates obtained from pet bird and chicken.

References

Horish RE. Ceftiofur use in food animals. Curr Top Med Chem 2002; 2: 717–731.

Timmerman T, Dewulf J, Catry B, Feyen B, Opsomer G, de Kruif A, Maes D. Quantification and evaluation of antimicrobial-drug use in group treatments for fattening pigs in Belgium. Prev Vet Med 2006; 74: 251–263.

Naseer U, and Sundsfjord A. The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. Microb Drug Resist 2011; 17: 83–97.

Horton RA, Randall LP, Snary EL, Cockrem H, Lotz S, Wearing H, Duncan D, Rabie A, McLaren I, Watson E, La Ragione RM, Coldham NG. Fecal carriage and shedding density of CTX-M extended-spectrum {beta}-lactamase-producing Escherichia coli in cattle, chickens, and pigs: Implications for environmental contamination and food production. Appl Environ Microbiol. 2011;77: 3715-37159.

Watson E, Jeckel S, Snow L, Stubbs R, Teale C, Wearing H, Horton R, Toszeghy M, Tearne O, Ellis-Iversen J, Coldham N. Epidemiology of extended spectrum beta-lactamase E. coli (CTX-M-15) on a commercial dairy farm. Vet. Microbiol. 2012; 154: 339–346.

Doi Y, Paterson DL, Egea P, Pascual A, López-Cerero L, Navarro MD, Adams-Haduch JM, Qureshi ZA, Sidjabat HE, Rodríguez-Baño J. Extended-spectrum and CMY-type beta-lactamase-producing Escherichia coli in clinical samples and retail meat from Pittsburgh, USA and Seville, Spain. Clin Microbiol Infect. 2010; 16: 33–38.

O'Keefe A, Hutton TA, Schifferli DM, Rankin SC. First detection of CTX-M and SHV extended-spectrum β-lactamases in Escherichia coli urinary tract isolates from dogs and cats in the United States. Antimicrob Agents Chemother. 2010; 54: 3489–3492.

Costa D, Poeta P, Sáenz Y, Vinué L, Rojo-Bezares B, Jouini A, Zarazaga M, Rodrigues J, Torres C. Detection of Escherichia coli harbouring extended-spectrum beta-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J Antimicrob Chemother. 2006; 58: 1311–1312.

Radhouani H, Pinto L, Coelho C, Gonçalves A, Sargo R, Torres C, Igrejas G, Poeta P. Detection of Escherichia coli harbouring extended-spectrum β-lactamases of the CTX-M classes in faecal samples of common buzzards (Buteo buteo). J Antimicrob Chemother. 2010; 65: 171–173.

Bindayna KM, Khanfar HS, Senok AC, Botta GA. Production of CTX-M genotype among ESBL-isolates in a tertiary hospital in Saudi Arabia. Saudi Med J. 2010; 31:859-863.

Hassan MI, Alkharsah KR, Alzahrani AJ, Obeid OE, Khamis AH, Diab A. Detection of extended spectrum beta-lactamases-producing isolates and effect of AmpC overlapping. J Infect Dev Ctries. 2013; 7(8): 618-629.

Hassan H, and Abdalhamid B. Molecular characterization of extended-spectrum beta-lactamase producing Enterobacteriaceae in a Saudi Arabian tertiary hospital. J Infect Dev Ctries. 2014; 8(3): 282-288.

Alekshun MN, and Levy SB. Molecular mechanisms of antibacterial multidrug resistance. Cell 2007; 128(6): 1037–1050.

Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational Supplement. CLSI document M100-S23 (ISBN 1-56238-865-7 [Print]; ISBN 1-56238-866-5 [Electronic]). Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087 USA, 2013.

Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis. 1998; 10: 867–878.

Pitout JD, Reisbig MD, Venter EC, Church DL, Hanson ND. Modification of the double-disk test for detection of Enterobacteriaceae producing extended spectrum and AmpC β-lactamases. J Clin Microbiol. 2003; 41: 3933–3935.

Chen J, and Griffiths NW PCR differentiation of Escherichia coli from other gram-negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. Lett Appl Microbiol. 1998; 27:369–371.

Fang H, Ataker F, Hedin G, Dornbusch K. Molecular epidemiology of extended-spectrum-lactamases among Escherichia coli isolates collected in a Swedish hospital and its associated health care facilities from 2001 to 2006. J Clin Microbiol. 2008; 46(2): 707–712.

Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 1990; 18(22):6531–6535.

Livermore DM, and Hawkey PM. CTX-M: Changing the face of ESBLs in the UK. J Antimicrob Chemother. 2005; 56: 451-454.

Wyllie DH, Baxter E, Morgan M, Bowller TC. Spread of multiresistance and extended-spectrum ß-lactamases amongst urinary Escherichia coli in Oxford, UK. J Antimicrob Chemother. 2005; 56: 986-988.

Canton R, Coque TM. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol. 2006; 9:466–475.

Liebana E, Batchelor M, Hopkins KL, Clifton-Hadley FA, Teale CJ, Foster A, Barker L, Threlfall EJ, Davies RH. Longitudinal farm study of extended-spectrum beta-lactamase-mediated resistance. J Clin Microbiol. 2006; 44: 1630–1634.

Tian GB, Wang HN, Zou LK, Tang JN, Zhao YW, Ye MY, Tang JY, Zhang Y, Zhang AY, Yang X, Xu CW, Fu YJ. Detection of CTX-M-15, CTX-M-22, and SHV-2 extended-spectrum beta-lactamases (ESBLs) in Escherichia coli fecal-sample isolates from pig farms in China. Foodborne Pathog Dis. 2009; 6: 297–304.

Duan RS, Sit THC, Wong SSY, Wong RCW, Chow KH, Mak GC, Ng LT, Yam WC, Yuen KY, Ho PL. Escherichia coli producing CTX-M-lactamases in food animals in Hong Kong. Microbes Drug Resist. 2006; 12: 145–148.

Costa D, Vinué L, Poeta P, Coelho AC, Matos M, Sáenz Y, Somalo S, Zarazaga M, Rodrigues J, Torres C. Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of broilers. Vet Microbiol. 2009; 138: 339-344.

Wittum TE, Mollenkopf DF, Daniels JB, Parkinson AE, Mathews JL, Fry PR, Abley MJ, Gebreyes WA. CTX-M-type extended-spectrum beta-lactamases present in Escherichia coli from the feces of cattle in Ohio, United States. Foodborne Pathog Dis. 2010; 7(12): 1575-1579.

Zheng H, Zeng Z, Chen S, Liu Y, Yao Q, Deng Y, Chen X, Lv L, Zhuo C, Chen Z, Liu JH. Prevalence and characterisation of CTX-M beta-lactamases amongst Escherichia coli isolates from healthy food animals in China. Int J Antimicrob Agents 2012; 39(4): 305-310.

Schmid A, Hormansdorfer S, Messelhausser U, Kasbohrer A, Sauter-Louis C, Mansfeld R. Prevalence of extended-spectrum beta-Lactamase-producing Escherichia coli on bavarian dairy and beef cattle farms. Appl Environ Microbiol. 2013; 79(9): 3027-3032.

Costa D, Poeta P, Brin˜as L., Sa´enz Y, Rodrigues J, Torres C. Detection of CTX-M-1 and TEM-52 beta-lactamases in Escherichia coli strains from healthy pets in Portugal. J. Antimicrob Chemother. 2004; 54: 960–961.

Costa, D., Poeta P, Sa´enz Y, Vinue´ L, Rojo-Bezares B, Jouini A, Zarazaga M, Rodrigues J., Torres C. Detection of Escherichia coli harbouring extended-spectrum-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J Antimicrob Chemother. 2007; 59: 1311–1312.

Pinto L., Radhouani H, Coelho C, Costa PM, Simo˜es R, Branda˜o RML, Torres C, Igrejas G, Poeta P. Genetic Detection of Extended-Spectrum-Lactamase-containing Escherichia coli Isolates from Birds of Prey from Serra da Estrela Natural Reserve in Portugal. Appl Environ microbial. 2010; 76(12): 4118–4120.

Bonnet R. Growing group of extended-spectrum-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother. 2004; 48:1–14.

Brinas, L., Lantero M, de Diego I, Alvarez M, Zarazaga M, Torres C. Mechanisms of resistance to expanded-spectrum cephalosporins in Escherichia coli isolates recovered in a Spanish hospital. J Antimicrob Chemother 2005; 56: 1107–1110.

Hu YY, Cai JC, Zhou HW, Chi D, Zhang XF, Chen WL, Zhang R, Chen GX. Molecular Typing of CTX-M-Producing Escherichia coli Isolates from Environmental Water, Swine Feces, Specimens from Healthy Humans, and Human Patients Appl Environ Microbiol. 2013; 79(19):5988–5996.

Al-Agamy MH, Shible AM, Hafez MM, AL-Ahdal MN, Memish ZA, Khubnani H. Molecular characteristics of extended-spectrum-producing Escherichia coli in Riyadh: emergence of CTX-M-15-producing Escherichia coli ST131. Annals Clin Microbiol Antimicrob. 2014; 13(4): 1-7.

Choi MJ, Lim SK, Jung SC, Ko KS. Comparison of CTX-M-producing Escherichia coli isolates from humans and animals in South Korea. J Bacteriol Virol. 2014; 44 (1): 44-51.

Xiong ZZ, Zhu DM, Wang F, Zhang YY. CTX-M-14, CTX-M-24 and resistance in Escherichia coli and Klebsiella pneumoniae clinical isolates. Chin Med J. 2006; 119: 160-164.

Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S, Kayser Y, Melhus A, Kahlmeter G, Waldenström J, Johansson A, Olsen B. Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the South of France. PloS One 2009; 4: e5958.

Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K, Huijsdens X, Kluytmans J. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis. 2011; 17: 1216-1222.

Stokes MO, Cottell JL, Piddock LJ, Wu G, Wootton M, Mevius DJ, Randall LP, Teale CJ, Fielder MD, Coldham NG. Detection and characterization of pCTlike plasmid vectors for blaCTX-M-14 in Escherichia coli isolates from humans, turkeys and cattle in England and Wales. J Antimicrob Chemother 2012; 67: 1639-1644.

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2015-10-21

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