Prevalence of Extended-Spectrum Beta-Lactamases in producing Escherichia coli in beef sold in traditional markets in Surabaya, Indonesia
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Abstract. Wardhana DK, Safitri DA, Anisa S, Harijani N, Estoepangestie S, Maghfiroh L. 2021. Prevalence of Extended-Spectrum Beta-Lactamases in producing Escherichia coli in beef sold in traditional markets in Surabaya, Indonesia. Biodiversitas 22: 2789-2793. Meat is a source of protein, but it can be contaminated by microorganisms such as Escherichia coli (E. coli). Some species of E. coli become resistant to antibiotics and produce Extended-Spectrum Beta-Lactamase (ESBL) that limit the choice of antibiotics for treatment of E. coli infection. The purpose of the study was to investigate the prevalence of ESBLs leading to the growth of Escherichia coli (E. coli) in beef sold in local markets in Surabaya City, Indonesia. A total of 60 samples from 10 traditional markets were tested. Isolated and identified E. coli strains were examined to detect the ESBL production through four-disc diffusion tests using cefotaxime (30 ?g), ceftazidime (30 ?g), ceftriaxone (30 ?g), and aztreonam (30 ?g). Then, the minimum inhibitory concentration was measured. The study showed the presence of ESBL-producing E. coli in beef sold in the traditional markets in Surabaya. The average E. coli concentration in the beef was at 43.3%, and the highest resistance of the isolates was observed for cefotaxime (46.1%), ceftazidime (23.1%) ceftriaxone (19.2%), and aztreonam (38.4%). Data of ESBL-producing E. coli in broiler chicken meat in the traditional markets showed all of the E. coli isolates were resistant to ampicillin, while 48.4% of them were resistant to, cephazolin. Only few (13%) were resistant to ceftazidime, and few others (9.6%) showed resistance to cefotaxime. The least number of them (6.4%) were resistant to ceftriaxone, and most of them were resistant to tetracycline (87.2%). Therefore, ESBLs were not reported producing E. coli in the beef. The presence of ESBL-producing E. coli in the beef gives an alert that good hygiene practices should be applied to handle meat safety and control the use of antibiotics
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References
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Niasono AB, Latif H, Purnawarman T. 2019. Antibiotic resistance to Escherichia coli bacteria isolated from broiler farms in Subang Regency, West Java. Jurnal Veteriner 20: 187-195.
Nyamakwere F, Muchenje V, Mushonga B, Makepe M, Mutero G. 2016. Assessment of Salmonella, Escherichia Coli, Enterobacteriaceae and Aerobic Colony Counts contamination levels during the beef slaughter process. Journal of Food Safety, 36(4), 548-556.
Nyirabahizi E, Tyson GH, Dessai U, Zhao S, Kabera C, Crarey E, Womack N, Crews MK, Strain E, Tate H. 2020. Evaluation of Escherichia coli as an indicator for antimicrobial resistance in Salmonella recovered from the same food or animal ceca samples. Food Control, 115, 107280.
Paredi G, Sentandreu MA, Mozzarelli A, Fadda S, Hollung K, de Almeida AM. 2013. .Muscle and meat: new horizons and applications for proteomics on a farm to fork perspective. Journal of Proteomics (88), 58–82.
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Raimondi S, Righini L, Candeliere F, Musmeci E, Bonvicini F, Gentilomi G, Erjavec MS, Amaretti A, Rossi M. 2019. Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. coli isolated from the feces of healthy subjects. Microorganisms, 7, 251.
Ramos S, Silva V, Dapkevicius MdLE, Canica M, Tejedor-Junco MT, Igrejas G, Poeta P. 2020. Escherichia coli as Commensal and Pathogenic Bacteria among Food-Producing Animals: Health Implications of Extended Spectrum Beta Lactamase (ESBL) Production. Animals, 10, 2239.
Soepranianondo K, Wardhana DK, Budiarto, Diyantoro. 2019. Analysis of bacterial contamination and antibiotic residue of beef meat from city slaughterhouses in East Java Province, Indonesia. Veterinary World 12(2): 243-248
Tan SL, Lee HY, Abu BF, Abdul KMS, Rukayadi Y, Mahyudin NA. 2013. Microbiological quality on food handlers hands at primary schools in Hulu Langat District, Malaysia. International Food Research Journal 20 (5): 2973- 2977
Valentin L, Sharp H, Hille K, Seibt U, Fischer J, Pfeifer Y, Michael GB, Nickel S, Schmiedel J, Falgenhauer L, Friese A, Bauerfeind R, Roesler U, Imirzalioglu C, Chakraborty T, Helmuth R, Valenza G, Werner G, Schwarz S, Guerra B, Appel B, Kreienbrock L, Käsbohrer A. 2014. Subgrouping of ESBL-producing Escherichia coli from animal and human sources: an approach to quantify the distribution of ESBL types between different reservoirs. Int. J. Med. Microbiol. 304, 805–816.
Widodo A, Effendi MH, Khairullah AR. 2020. Extendedspectrum beta-lactamase(ESBL)-producing Eschericia coli from livestock. Sys Rev Pharm, 2020; 11 (7): 382, 392.
Yang X, He A, Badoni M, Tran F, Wang H. 2017. Mapping sources of contamination of Escherichia coli on beef in the fabrication facility of a commercial beef packing plant. Food Control, 75, 153-159.
Yusha’u M and Umar MI. 2016. Phenotypic detection of extended-spectrum beta-lactamases in bacterial isolates from meat products sold within Kaduna Metropolis in Nigeria. Proceeding of International Conference on Biodiversity Society for Indonesian Biodiversity. Sebelas Maret University, Surakarta, 14-16 January 2016. [Indonesian]
Zafar A, Ahmed E, Wajiha, H, Khan A. 2016. Microbiological evaluation of raw meat products available in local markets of Karachi, Pakistan. Pakistan Academy of Sciences B. Life and Environmental Sciences, 53(2), 103-109.
Akbar A, Anal KA. 2013. Prevalence and antibiogramstudy of Salmonella and Staphylococcus aureusin poultry meat. Asian Pacifc Journal of Tropical Biomedicine. 3(2): 163-168.
Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol. 8(4): 251–259.
Aslanta? Ö., Elmac?o?lu S., Y?lmaz, E. ?. 2017. Prevalence and characterization of ESBL-and AmpC-producing Escherichia coli from cattle. Kafkas Univ Vet Fak Derg, 23, 63-67.
Bahri S., Rokhim S., Prasiska Y. S. 2019. Kontaminasi bakteri Escherichia coli pada sampel daging. Journal of Health Science and Prevention, 3(1), 62-67.
Bantawa K., Rai K., Limbu D. S., Khanal H. 2018. Food-borne bacterial pathogens in marketed raw meat of Dharan, eastern Nepal. BMC research notes, 11(1), 1-5.
Blaak H., Lynch, G., Italiaander, R., Hamidjaja, R. A., Schets, F. M., de Roda Husman, A. M. 2015. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One, 10(6), e0127752.
Chaisatit C., Tribuddharat C., Pulsrikarn C., Dejsirilert S. 2012. Molecular characterization of antibiotic-resistant bacteria in contaminated chicken meat sold at supermarkets in Bangkok, Thailand. Japanese journal of infectious diseases, 65(6), 527-534.
Chen C.M., Ke S.C., Li C.R., Wu Y.C., Chen T.H., Lai C.H., Wu L.T. 2017. High Diversity of Antimicrobial Resistance Genes, Class 1 Integrons, and Genotypes of Multidrug-Resistant Escherichia coli in Beef Carcasses. Microbial Drug Resistance, 23(7), 915–924. doi:10.1089/mdr.2016.0223
CLSI. 2017. M100 Performance Standards for Antimicrobial, 27th ed. Clinical and Laboratory Standards Institute, USA.
Effendi M. H., Cicilia R., Rahmahani J., Tyasningsih W. 2020. Public Awareness for Antimicrobial Resistance from Escherichia coli Isolated from Beef Sold on Several Wet Market in Surabaya, Indonesia. Indian Journal of Public Health Research & Development, 11(9).
Eyi A., Arslan S. 2012. Prevalence of Escherichia coli in retail poultry meat, ground beef and beef. Med. Weter, 68(4), 238.
Geser N., Stephan R., Hächler, H. 2012. Occurrence and characteristics of extended-spectrum ?-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC veterinary research, 8(1), 1-9.
Harlia E. 2017. Food Safety on Meat Products Based on Coliform Contamination. In International Seminar on Tropical Animal Production (ISTAP). 395-399.
Hemalata VB and Virupakshaiah DBM. 2016. Isolation and identification of food borne pathogens from spoiled food samples. International Journal of Current Microbiology and Applied Sciences 5(6), 1017–1025.
Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, Lago BA, Dave BM, Pereira S, Sharma AN. 2017. Expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45(D1):D566–D573.
Kaesbohrer A., Bakran-Lebl K., Irrgang A., Fischer J., Kämpf P., Schiffmann A., Werckenthin C., Busch M., Kreienbrock, L, Hille, K., 2019. Diversity in prevalence and characteristics of ESBL/pAmpC producing E. coli in food in Germany. Veterinary microbiology, 233, 52-60.
Kassem II., Nasser NA, Salibi J. 2020. Prevalence and Loads of Fecal Pollution Indicators and the Antibiotic Resistance Phenotypes of Escherichia coli in Raw Minced Beef in Lebanon. Foods, 9(11), 1543.
Kim YJ, Moon JS, Oh DH., Chon JW, Song BR, Lim JS, Sung K. 2018. Genotypic characterization of ESBL-producing E. coli from imported meat in South Korea. Food Research International, 107, 158-164.
Lindstedt BA, Finton MD, Porcellato D, Brandal LT. 2018. High frequency of hybrid Escherichia coli strains with combined Intestinal Pathogenic Escherichia coli (IPEC) and Extraintestinal Pathogenic Escherichia coli (ExPEC) virulence factors isolated from human faecal samples. BMC Infect. Dis. 18, 544.
Marshall BM, Levy SB. 2011. Food animals and antimicrobials: impacts on human health. Clinical microbiology reviews, 24(4), 718-733.
Martínez-Chávez L, Cabrera-Diaz E, Pérez-Montaño JA, Garay-Martínez LE, Varela-Hernández JJ, Castillo A, Martínez-Gonzáles NE. 2015. Quantitative distribution of Salmonella spp. and Escherichia coli on beef carcasses and raw beef at retail establishments. International Journal of Food Microbiology, 210, 149-155.
Moawad AA, Hotzel H, Awad O, Tomaso H, Neubauer H, Hafez HM, El-Adawy, H. 2017. Occurrence of Salmonella enterica and Escherichia coli in raw chicken and beef meat in northern Egypt and dissemination of their antibiotic resistance markers. Gut pathogens, 9(1), 57.
Montso KP, Dlamini SB, Kumar A, Ateba CN. 2019. Antimicrobial Resistance Factors of Extended-Spectrum-Beta-Lactamases Producing Escherichia coli and Klebsiella pneumoniae Isolated from Cattle Farms and Raw Beef in North-West Province, South Africa. BioMed Research International Volume 2019
Niasono AB, Latif H, Purnawarman T. 2019. Antibiotic resistance to Escherichia coli bacteria isolated from broiler farms in Subang Regency, West Java. Jurnal Veteriner 20: 187-195.
Nyamakwere F, Muchenje V, Mushonga B, Makepe M, Mutero G. 2016. Assessment of Salmonella, Escherichia Coli, Enterobacteriaceae and Aerobic Colony Counts contamination levels during the beef slaughter process. Journal of Food Safety, 36(4), 548-556.
Nyirabahizi E, Tyson GH, Dessai U, Zhao S, Kabera C, Crarey E, Womack N, Crews MK, Strain E, Tate H. 2020. Evaluation of Escherichia coli as an indicator for antimicrobial resistance in Salmonella recovered from the same food or animal ceca samples. Food Control, 115, 107280.
Paredi G, Sentandreu MA, Mozzarelli A, Fadda S, Hollung K, de Almeida AM. 2013. .Muscle and meat: new horizons and applications for proteomics on a farm to fork perspective. Journal of Proteomics (88), 58–82.
Poirel L, Madec JY, Lupo A, Schink AK, Kieffer N, Nordmann P, Schwarz S. 2018. Antimicrobial resistance in Escherichia coli. Antimicrobial resistance in bacteria from livestock and companion animals, pp.289-316
Rahman MA, Rahman AK, Islam MA, Alam MM. 2017. Antimicrobial resistance of Escherichia coli isolated from milk, beef and chicken meat in Bangladesh. Bangladesh Journal of Veterinary Medicine, 15(2), 141-146.
Raimondi S, Righini L, Candeliere F, Musmeci E, Bonvicini F, Gentilomi G, Erjavec MS, Amaretti A, Rossi M. 2019. Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. coli isolated from the feces of healthy subjects. Microorganisms, 7, 251.
Ramos S, Silva V, Dapkevicius MdLE, Canica M, Tejedor-Junco MT, Igrejas G, Poeta P. 2020. Escherichia coli as Commensal and Pathogenic Bacteria among Food-Producing Animals: Health Implications of Extended Spectrum Beta Lactamase (ESBL) Production. Animals, 10, 2239.
Soepranianondo K, Wardhana DK, Budiarto, Diyantoro. 2019. Analysis of bacterial contamination and antibiotic residue of beef meat from city slaughterhouses in East Java Province, Indonesia. Veterinary World 12(2): 243-248
Tan SL, Lee HY, Abu BF, Abdul KMS, Rukayadi Y, Mahyudin NA. 2013. Microbiological quality on food handlers hands at primary schools in Hulu Langat District, Malaysia. International Food Research Journal 20 (5): 2973- 2977
Valentin L, Sharp H, Hille K, Seibt U, Fischer J, Pfeifer Y, Michael GB, Nickel S, Schmiedel J, Falgenhauer L, Friese A, Bauerfeind R, Roesler U, Imirzalioglu C, Chakraborty T, Helmuth R, Valenza G, Werner G, Schwarz S, Guerra B, Appel B, Kreienbrock L, Käsbohrer A. 2014. Subgrouping of ESBL-producing Escherichia coli from animal and human sources: an approach to quantify the distribution of ESBL types between different reservoirs. Int. J. Med. Microbiol. 304, 805–816.
Widodo A, Effendi MH, Khairullah AR. 2020. Extendedspectrum beta-lactamase(ESBL)-producing Eschericia coli from livestock. Sys Rev Pharm, 2020; 11 (7): 382, 392.
Yang X, He A, Badoni M, Tran F, Wang H. 2017. Mapping sources of contamination of Escherichia coli on beef in the fabrication facility of a commercial beef packing plant. Food Control, 75, 153-159.
Yusha’u M and Umar MI. 2016. Phenotypic detection of extended-spectrum beta-lactamases in bacterial isolates from meat products sold within Kaduna Metropolis in Nigeria. Proceeding of International Conference on Biodiversity Society for Indonesian Biodiversity. Sebelas Maret University, Surakarta, 14-16 January 2016. [Indonesian]
Zafar A, Ahmed E, Wajiha, H, Khan A. 2016. Microbiological evaluation of raw meat products available in local markets of Karachi, Pakistan. Pakistan Academy of Sciences B. Life and Environmental Sciences, 53(2), 103-109.
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