Skip to main content
Top
Published in: BMC Public Health 1/2016

Open Access 01-12-2016 | Research article

Risk factors and spatial distribution of extended spectrum β-lactamase-producing- Escherichia coli at retail poultry meat markets in Malaysia: a cross-sectional study

Authors: A. B. Aliyu, A. A. Saleha, A. Jalila, Z. Zunita

Published in: BMC Public Health | Issue 1/2016

Login to get access

Abstract

Background

The significant role of retail poultry meat as an important exposure pathway for the acquisition and transmission of extended spectrum β-lactamase-producing Escherichia coli (ESBL-EC) into the human population warrants understanding concerning those operational practices associated with dissemination of ESBL-EC in poultry meat retailing. Hence, the objective of this study was to determine the prevalence, spatial distribution and potential risk factors associated with the dissemination of ESBL-EC in poultry meat retail at wet-markets in Selangor, Malaysia.

Methods

Poultry meat (breast, wing, thigh, and keel) as well as the contact surfaces of weighing scales and cutting boards were sampled to detect ESBL-EC by using culture and disk combination methods and polymerase chain reaction assays. Besides, questionnaire was used to obtain data and information pertaining to those operational practices that may possibly explain the occurrence of ESBL-EC. The data were analysed using logistic regression analysis at 95 % CI.

Results

The overall prevalence of ESBL-EC was 48.8 % (95 % CI, 42 – 55 %). Among the risk factors that were explored, type of countertop, sanitation of the stall environment, source of cleaning water, and type of cutting board were found to be significantly associated with the presence of ESBL-EC.

Conclusions

Thus, in order to prevent or reduce the presence of ESBL-EC and other contaminants at the retail-outlet, there is a need to design a process control system based on the current prevailing practices in order to reduce cross contamination, as well as to improve food safety and consumer health.
Appendix
Available only for authorised users
Literature
3.
go back to reference Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, Bender J, Smith KE, Winokur PL, Belongia EA. Antimicrobial drug–resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis. 2007;13(6):838.CrossRefPubMedPubMedCentral Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA, Bender J, Smith KE, Winokur PL, Belongia EA. Antimicrobial drug–resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis. 2007;13(6):838.CrossRefPubMedPubMedCentral
4.
go back to reference Vieira AR, Collignon P, Aarestrup FM, McEwen SA, Hendriksen RS, Hald T, Wegener HC. Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study. Foodborne Pathog Dis. 2011;8(12):1295–301.CrossRefPubMed Vieira AR, Collignon P, Aarestrup FM, McEwen SA, Hendriksen RS, Hald T, Wegener HC. Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: an ecological study. Foodborne Pathog Dis. 2011;8(12):1295–301.CrossRefPubMed
5.
go back to reference Schwaber MJ, Navon-Venezia S, Kaye KS, Ben-Ami R, Schwartz D, Carmeli Y. Clinical and economic impact of bacteremia with extended-spectrum-β-lactamase-producing Enterobacteriaceae. Antimicrob Agents Chemother. 2006;50(4):1257–62.CrossRefPubMedPubMedCentral Schwaber MJ, Navon-Venezia S, Kaye KS, Ben-Ami R, Schwartz D, Carmeli Y. Clinical and economic impact of bacteremia with extended-spectrum-β-lactamase-producing Enterobacteriaceae. Antimicrob Agents Chemother. 2006;50(4):1257–62.CrossRefPubMedPubMedCentral
6.
go back to reference De Kraker MEA, Wolkewitz M, Davey PG, Koller W, Berger J, Nagler J, Grundmann H. Burden of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay associated with bloodstream infections due to Escherichia coli resistant to third-generation cephalosporins. J Antimicrob Chemother. 2011;66(2):398–407.CrossRefPubMed De Kraker MEA, Wolkewitz M, Davey PG, Koller W, Berger J, Nagler J, Grundmann H. Burden of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay associated with bloodstream infections due to Escherichia coli resistant to third-generation cephalosporins. J Antimicrob Chemother. 2011;66(2):398–407.CrossRefPubMed
7.
go back to reference Aidara-Kane A, Andremont A, Collignon P. Antimicrobial resistance in the food chain and the AGISAR initiative. J Infect Public Health. 2013;6(3):162–5.CrossRefPubMed Aidara-Kane A, Andremont A, Collignon P. Antimicrobial resistance in the food chain and the AGISAR initiative. J Infect Public Health. 2013;6(3):162–5.CrossRefPubMed
8.
go back to reference Jury KL, Vancov T, Stuetz RM, Khan SJ. Antibiotic resistance dissemination and sewage treatment plants. Curr Res Technol Edu Topics Appl Microbiol and Microbial Biotechnol. 2010;2:509–10. Jury KL, Vancov T, Stuetz RM, Khan SJ. Antibiotic resistance dissemination and sewage treatment plants. Curr Res Technol Edu Topics Appl Microbiol and Microbial Biotechnol. 2010;2:509–10.
9.
go back to reference Sekawi Z, Yusof R, Shamsudin MN. Extended-Spectrum β-Lactamases-Producing Escherichia coli from a Tertiary Hospital in Malaysia: Emergence of CTX-M-Type β-Lactamases Variation. Res J Microbiol. 2008;3(6):489–93.CrossRef Sekawi Z, Yusof R, Shamsudin MN. Extended-Spectrum β-Lactamases-Producing Escherichia coli from a Tertiary Hospital in Malaysia: Emergence of CTX-M-Type β-Lactamases Variation. Res J Microbiol. 2008;3(6):489–93.CrossRef
10.
go back to reference Hashim RB, Husin S, Rahman MM. Detection of β-lactamase producing bacterial genes and their clinical features. Pak J Biol Sci. 2011;14(1):41.CrossRefPubMed Hashim RB, Husin S, Rahman MM. Detection of β-lactamase producing bacterial genes and their clinical features. Pak J Biol Sci. 2011;14(1):41.CrossRefPubMed
11.
go back to reference Costa D, Vinué L, Poeta P, Coelho AC, Matos M, Sáenz Y, Torres C. Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of broilers. Vet Microbiol. 2009;138(3):339–44.CrossRefPubMed Costa D, Vinué L, Poeta P, Coelho AC, Matos M, Sáenz Y, Torres C. Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolates in faecal samples of broilers. Vet Microbiol. 2009;138(3):339–44.CrossRefPubMed
12.
go back to reference Stuart JC, van den Munckhof T, Voets G, Scharringa J, Fluit A, Leverstein-Van Hall M. Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol. 2012;154(3):212–4.CrossRef Stuart JC, van den Munckhof T, Voets G, Scharringa J, Fluit A, Leverstein-Van Hall M. Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol. 2012;154(3):212–4.CrossRef
18.
go back to reference Cools I, Uyttendaele M, Cerpentier J, D'haese E, Nelis HJ, Debevere J. Persistence of Campylobacter jejuni on surfaces in a processing environment and on cutting boards. Lett Appl Microbiol. 2005;40(6):418–23.CrossRefPubMed Cools I, Uyttendaele M, Cerpentier J, D'haese E, Nelis HJ, Debevere J. Persistence of Campylobacter jejuni on surfaces in a processing environment and on cutting boards. Lett Appl Microbiol. 2005;40(6):418–23.CrossRefPubMed
19.
go back to reference MR U, Maarof F, Robin T, Chai LC, Cheah YK, Mohamad Ghazali F, Radu S. Occurrence and antibiotic resistance of Campylobacter jejuni and Campylobacter coli in retail broiler chicken. Inter Food Res J. 2010;17(2):247–55. MR U, Maarof F, Robin T, Chai LC, Cheah YK, Mohamad Ghazali F, Radu S. Occurrence and antibiotic resistance of Campylobacter jejuni and Campylobacter coli in retail broiler chicken. Inter Food Res J. 2010;17(2):247–55.
20.
go back to reference Philippe L, Franil T, Patricia B, George GZ, Daryl JH. Evaluation of a chromogenic medium for extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae. Canada: University of Manitoba; 2010. ECCMID, Vienna, Austria 10 – 13 April 2010. Philippe L, Franil T, Patricia B, George GZ, Daryl JH. Evaluation of a chromogenic medium for extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae. Canada: University of Manitoba; 2010. ECCMID, Vienna, Austria 10 – 13 April 2010.
21.
go back to reference Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk susceptibility tests. Approved standard, 10th ed. CLSI document M02-A10. Wayne, PA: CLSI; 2010. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk susceptibility tests. Approved standard, 10th ed. CLSI document M02-A10. Wayne, PA: CLSI; 2010.
22.
go back to reference Hawkey PM. Prevalence and clonality of extended‐spectrum β‐lactamases in Asia. Clin Microbiol Infec. 2008;14(s1):159–65.CrossRef Hawkey PM. Prevalence and clonality of extended‐spectrum β‐lactamases in Asia. Clin Microbiol Infec. 2008;14(s1):159–65.CrossRef
23.
go back to reference Hawser SP, Bouchillon SK, Hoban DJ, Badal RE, Hsueh PR, Paterson DL. Emergence of high levels of extended-spectrum-β-lactamase-producing gram-negative bacilli in the Asia-Pacific region: data from the Study for Monitoring Antimicrobial Resistance Trends (SMART) program, 2007. Antimicrob Agents Chemother. 2009;53(8):3280–4.CrossRefPubMedPubMedCentral Hawser SP, Bouchillon SK, Hoban DJ, Badal RE, Hsueh PR, Paterson DL. Emergence of high levels of extended-spectrum-β-lactamase-producing gram-negative bacilli in the Asia-Pacific region: data from the Study for Monitoring Antimicrobial Resistance Trends (SMART) program, 2007. Antimicrob Agents Chemother. 2009;53(8):3280–4.CrossRefPubMedPubMedCentral
24.
go back to reference Lahmer RA, Williams AP, Townsend S, Baker S, Jones DL. Antibacterial action of chitosan-arginine against Escherichia coli O157 in chicken juice. Food Control. 2012;26(1):206–11.CrossRef Lahmer RA, Williams AP, Townsend S, Baker S, Jones DL. Antibacterial action of chitosan-arginine against Escherichia coli O157 in chicken juice. Food Control. 2012;26(1):206–11.CrossRef
25.
go back to reference Mataragas M, Skandamis PN, Drosinos EH. Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. Int J Food Microbiol. 2008;126(1):1–12.CrossRefPubMed Mataragas M, Skandamis PN, Drosinos EH. Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. Int J Food Microbiol. 2008;126(1):1–12.CrossRefPubMed
26.
go back to reference Wong T, Janet Whyte R, Joyce Cornelius A, Hudson JA. Enumeration of Campylobacter and Salmonella on chicken packs. Br Food J. 2004;106(9):651–62.CrossRef Wong T, Janet Whyte R, Joyce Cornelius A, Hudson JA. Enumeration of Campylobacter and Salmonella on chicken packs. Br Food J. 2004;106(9):651–62.CrossRef
27.
go back to reference Zhu J, Wang Y, Song X, Cui S, Xu H, Yang B, Li F. Prevalence and quantification of Salmonella contamination in raw chicken carcasses at the retail in China. Food Control. 2014;44:198–202.CrossRef Zhu J, Wang Y, Song X, Cui S, Xu H, Yang B, Li F. Prevalence and quantification of Salmonella contamination in raw chicken carcasses at the retail in China. Food Control. 2014;44:198–202.CrossRef
28.
go back to reference Burgess F, Little CL, Allen G, Williamson K, Mitchell RT. Prevalence of Campylobacter, Salmonella, and Escherichia coli on the external packaging of raw meat. J Food Prot. 2005;68(3):469–75.PubMed Burgess F, Little CL, Allen G, Williamson K, Mitchell RT. Prevalence of Campylobacter, Salmonella, and Escherichia coli on the external packaging of raw meat. J Food Prot. 2005;68(3):469–75.PubMed
29.
go back to reference Mather AE, Reid SWJ, McEwen SA, Ternent HE, Reid-Smith RJ, Boerlin P, Mellor DJ. Factors associated with cross-contamination of hides of Scottish cattle by Escherichia coli O157. Appl Environ Microbiol. 2008;74(20):6313–9.CrossRefPubMedPubMedCentral Mather AE, Reid SWJ, McEwen SA, Ternent HE, Reid-Smith RJ, Boerlin P, Mellor DJ. Factors associated with cross-contamination of hides of Scottish cattle by Escherichia coli O157. Appl Environ Microbiol. 2008;74(20):6313–9.CrossRefPubMedPubMedCentral
30.
go back to reference Harrison WA, Griffith CJ, Tennant D, Peters AC. Incidence of Campylobacter and Salmonella isolated from retail chicken and associated packaging in South Wales. Lett Appl Microbiol. 2001;33(6):450–4.CrossRefPubMed Harrison WA, Griffith CJ, Tennant D, Peters AC. Incidence of Campylobacter and Salmonella isolated from retail chicken and associated packaging in South Wales. Lett Appl Microbiol. 2001;33(6):450–4.CrossRefPubMed
31.
go back to reference Ismaïl R, Aviat F, Michel V, Le Bayon I, Gay-Perret P, Kutnik M, Fédérighi M. Methods for recovering microorganisms from solid surfaces used in the food industry: a review of the literature. Int J Environ Res Public Health. 2013;10(11):6169–83.CrossRefPubMedPubMedCentral Ismaïl R, Aviat F, Michel V, Le Bayon I, Gay-Perret P, Kutnik M, Fédérighi M. Methods for recovering microorganisms from solid surfaces used in the food industry: a review of the literature. Int J Environ Res Public Health. 2013;10(11):6169–83.CrossRefPubMedPubMedCentral
32.
go back to reference Moore G, Blair IS, McDowell DA. Recovery and transfer of Salmonella typhimurium from four different domestic food contact surfaces. J Food Prot. 2007;70(10):2273–80.PubMed Moore G, Blair IS, McDowell DA. Recovery and transfer of Salmonella typhimurium from four different domestic food contact surfaces. J Food Prot. 2007;70(10):2273–80.PubMed
33.
go back to reference Tang JYH, Nishibuchi M, Nakaguchi Y, Ghazali FM, Saleha AA, Son R. Transfer of Campylobacter jejuni from raw to cooked chicken via wood and plastic cutting boards. Lett Appl Microbiol. 2011;52(6):581–8.CrossRefPubMed Tang JYH, Nishibuchi M, Nakaguchi Y, Ghazali FM, Saleha AA, Son R. Transfer of Campylobacter jejuni from raw to cooked chicken via wood and plastic cutting boards. Lett Appl Microbiol. 2011;52(6):581–8.CrossRefPubMed
34.
go back to reference Pérez-Rodríguez F, Castro R, Posada-Izquierdo GD, Valero A, Carrasco E, García-Gimeno RM, Zurera G. Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail. Meat Sci. 2010;86(2):479–85.CrossRefPubMed Pérez-Rodríguez F, Castro R, Posada-Izquierdo GD, Valero A, Carrasco E, García-Gimeno RM, Zurera G. Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail. Meat Sci. 2010;86(2):479–85.CrossRefPubMed
35.
go back to reference Kusumaningrum HD, Riboldi G, Hazeleger WC, Beumer RR. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol. 2003;85(3):227–36.CrossRefPubMed Kusumaningrum HD, Riboldi G, Hazeleger WC, Beumer RR. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol. 2003;85(3):227–36.CrossRefPubMed
Metadata
Title
Risk factors and spatial distribution of extended spectrum β-lactamase-producing- Escherichia coli at retail poultry meat markets in Malaysia: a cross-sectional study
Authors
A. B. Aliyu
A. A. Saleha
A. Jalila
Z. Zunita
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2016
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-016-3377-2

Other articles of this Issue 1/2016

BMC Public Health 1/2016 Go to the issue