Identification of BlaTEM Gene Encode Extended Spectrum Beta Lactamase (ESBL) Producing Escherichia coli Isolated from Fresh Beef

Lailatul Maghfiroh, Mustofa Helmi Effendi, Wiwiek Tyasningsih, Adiana Mutamsari Witaningrum, Agumah Nnabuife Bernard

Abstract


Background: The community needs fresh beef of good quality. Dirty sanitation causes Escherichia coli to easily contaminate fresh meat and E. coli is one of the bacteria that can produce ESBL enzymes that impact human health. This study aimed to isolate Escherichia coli from fresh meat at the Surabaya Traditional Markets to identify the presence of the ESBL-encoding blaTEM gene.

Methods: One hundred fifty fresh beef samples were collected from six traditional markets located in Surabaya city. Then, a polymerase chain reaction (PCR) test was performed to detect the blaTEM gene which codes for ESBL in isolates that unveiled positive results for MDR (resistant to three antibiotics) and suspected beta-lactamase enzyme (resistant to ampicillin).

Results: The research showed that from 150 samples of fresh beef at the Surabaya Traditional Market, 68 Escherichia coli isolates were found (45.3%). Escherichia coli isolates were shown to be susceptible to the antibiotic’s ampicillin (73.5%), gentamicin (95%), tetracycline (7.5%), aztreonam (100%), and ciprofloxacin (95%). The highest percentage of resistance of Escherichia coli isolates to the antibiotic ampicillin (19.1%). PCR analysis of ampicillin-resistant isolates showed that the blaTEM gene encoding ESBL was present in 7 (53.8%) of the 13 Escherichia coli isolates.

Conclusion: The research results show that there is a risk of ESBL transmission to the community through Escherichia coli which was identified in fresh beef at the Surabaya Traditional Market. Therefore, it is hoped that public awareness can increase regarding food safety issues which can have an impact on public health.

Keywords: Escherichia coliblaTEM; ESBL; Fresh beef; Public health  


Full Text:

PDF

References


Nüesch-Inderbinen M, Kindle P, Baschera M, Liljander A, Jores J, et al.. Antimicrobial resistant and extended-spectrum β-lactamase (ESBL) producing Escherichia coli isolated from fecal samples of African dromedary camels. Scientific African, (2020); 7: e00274 .

Yanestria SM, Dameanti FNAEP, Musayannah BG, Pratama JWA, Witaningrum AM, et al. Antibiotic resistance pattern of Extended-Spectrum β-Lactamase (ESBL) producing Escherichia coli isolated from broiler farm environment in Pasuruan district, Indonesia. Biodiversitas: Journal of Biological Diversity, (2022); 23(9): 4460–4465.

Effendi MH, Tyasningsih W, Yurianti YA, Rahmahani J, Harijani N, et al. Presence of multidrug resistance (MDR) and extended-spectrum beta-lactamase (ESBL) of Escherichia coli isolated from cloacal swabs of broilers in several wet markets in Surabaya, Indonesia. Biodiversitas, (2021); 22(1): 304–310.

Wibisono FJ, Sumiarto B, Untari T, Effendi MH, Permatasari DA, et al. Molecular identification of CTX gene of extended spectrum beta-lactamases (ESBL) producing Escherichia coli on layer chicken in Blitar, Indonesia. Journal of Animal and Plant Sciences, (2021); 31(4): 954–959.

Effendi MH, Faridah HD, Wibisono FM, Wibisono FJ, Nisa N, et al. Detection of virulence factor encoding genes on Escherichia coli isolated from broiler chicken in Blitar District, Indonesia. Biodiversitas: Journal of Biological Diversity, (2022); 23(7): 3437-3442.

Tyasningsih W, Ramandinianto SC, Ansharieta R, Witaningrum AM, Permatasari DA, et al. Prevalence and antibiotic resistance of Staphylococcus aureus and Escherichia coli isolated from raw milk in East Java, Indonesia. Veterinary World, (2022); 15(8): 2021–2028.

Shabana II, Al-Enazi AT. Investigation of plasmid-mediated resistance in Escherichia coli isolated from healthy and diarrheic sheep and goats. Saudi Journal of Biological Sciences, (2020); 27(3): 788–796.

Karacan Sever N, Sahan Yapicier O, Akan M. Distribution of Serotypes and Antibiotic Resistance of Avian Pathogenic Escherichia coli Strains Isolated from Chickens. Kafkas Universitesi Veteriner Fakultesi Dergisi, (2022); 28(6): 767-772.

Ansharieta R, Ramandinianto SC, Effendi MH, Plumeriastuti H. Molecular identification of blaCTX-M and blaTEM genes encoding extended spectrum beta-lactamase (ESBL) producing Escherichia coli isolated from raw cow’s milk in East Java Indonesia. Biodiversitas, (2021); 22(4): 1600–1605.

Imasari T. Prevalence and Genotypic Patterns of SHV, TEM, CTX-M Bacteria Enterobacteriaceae Produce Extended Spectrum β-Lactamase from Dairy Cow Feces and Residents Around Livestock in Surabaya. Thesis. (2017).

Mensah DO, Noah ON, Evelyn YB, Ebenezer OM, Kingsley ID, et al. (2016) Genetic characterization of TEM-type ESBL-associated antibacterial resistance in Enterobacteriaceae in a tertiary hospital in Ghana. Annals of Clinical Microbiology and Antimicrobials, (2016); 15(29): 1–9.

Dirar MH, Bilal NE, Ibrahim ME, Hamid ME. Prevalence of extended-spectrum Beta-lactamase (ESBL) and molecular detection of blaTEM, blaSHV, and blaCTX-M genotypes among Enterobacteriaceae isolates from patients in Khartoum, Sudan. Pan African Medical Journal, (2020); 37(213): Page numbers not for citation purposes.

Naelasari DN, Koendhori EB, Dewanti L, Sulistiawati Sarassari R, Kuntaman, K. The Prevalence of Extended Spectrum Beta Lactamase (ESBL) Producing Gut Bacterial Flora among Patients in Dr. Soetomo Hospital and Primary Health Center in Surabaya. Folia Medica Indonesiana, (2018); 54(4): 256–262.

Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of TEM, SHV, and CTX M Beta Lactamase genes in the urinary isolates of a tertiary care hospital. The Avicenna Medical Journal, (2017); 7(1): 12–16.

Wayne PA, Methods for Dilution Antimicrobial Susceptibility Test for Bacteria that Grow Aerobically, https://clsi.org/media/1928/m07ed11_sample.pdf, (Accessed: 2.9.2024).

Eyi A, Arslan S. Prevalence of Escherichia coli in retail poultry meat, ground beef and beef. Med. Weter, (2012); 68(4): 237–240.

Langgar SMC, Sanam MUE, Annitha IR, Detha D. Prevalence of Escherichia coli in Beef in Oeba Slaughterhouse, Kupang City. Jurnal Veteriner Nusantara, (2021); 4(1): 1–10.

Guo S, Aung KT, Lee P, Tay MYF, Seow KLG, et al. Prevalence and genomic analysis of ESBL-producing Escherichia coli in retail raw meats in Singapore. Journal of Antimicrobial Chemotherapy, (2020); 76(3): 601–605.

Sulaxono H. Escherichia coli Contamination on Fresh Meat in the Working Area of the Maros Veterinary Center. Proceedings of the National Seminar on Animal and Veterinary Technology, (2020); 906–913.

Indraswari A, Dyah AW, Aris H, I Wayan S. Escherichia coli diarrhea in Beef in the Special Region of Yogyakarta and the Pattern of Resistance to Antibiotics. (2022).

Adzitey, F. Incidence and antimicrobial susceptibility of Escherichia coli isolated from beef (meat muscle, liver, and kidney) samples in Wa Abattoir, Ghana. Cogent Food & Agriculture, (2020); 6(1): 1718269.

Ramos S, Silva V, Dapkevicius MLE, Caniça M, Junco MTT, et al. Escherichia coli as Commensal and Pathogenic Bacteria among Food-Producing Animals: Health Implications of Extended Spectrum β-Lactamase (ESBL) Production. Animals, (2020); 10(12): 2239.

Poirel L, Madec JY, Lupo A, Schink AK, Kieffer N, et al. Antimicrobial Resistance in Escherichia coli. Microbiology Spectrum, (2018); 6(4): ARBA-0026-2017.

Hassuna NA, Khairalla AS, Farahat EM, Hammad AM, Fattah MA. Molecular characterization of Extended-spectrum β-lactamase producing Escherichia coli recovered from community-acquired urinary tract infections in Upper Egypt. Scientific Reports, (2020); 10 (1): 2772.

Geser N, Stephan R, Hachler H. Occurrence and characteristics of extended-spectrum-β-lactamase (ESBL) producing Enterobacteriaceae in Food-producing animals, minced meat and raw milk. BMC Veterinary Research, (2012); 8(21): 1–9.

Abayneh M, Tesfaw G, Woldemichael K, Yohannis M, Abdissa A. Assessment of extended-spectrum β-lactamase (ESBLs) – producing Escherichia coli from minced meat of cattle and swab samples and hygienic status of meat retailer shops in Jimma town, Southwest Ethiopia. BMC Infectious Diseases, (2019); 19: 1–8.

Haile AF, Alonso S, Berhe N, Atoma TB, Boyaka PN, et al. Prevalence, Antibiogram, and Multidrug-Resistant Profile of E. coli O157: H7 in Retail Raw Beef in Addis Ababa, Ethiopia. Frontiers in Veterinary Science, (2022); 9: 734896.

Palmeira JD, Haenni M, Matayer V, Madec JY, Ferreira HMN. Epidemic spread of IncI1/pST113 plasmid carrying the Extended-Spectrum Beta-Lactamase (ESBL) blaCTX-M-8 gene in Escherichia coli of Brazilian cattle. Veterinary Microbiology, (2020); 243: 108629.

Michael GB, Kaspar H, Siqueira AK, Costa EF, Corbellini LG, et al. Extended-spectrum b-lactamase (ESBL)-producing Escherichia coli isolates collected from diseased food-producing animals in the GERM-Vet monitoring program 2008–2014. Veterinary Microbiology, (2017); 200: 142–150.

Montso KP, Dlamini SB, Kumar A, Ateba CN. 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, (2019); 2019(1): 1–13.

Syahmifariza, Indrawati N, Supriatna A, Faith, Sensitivity Test of Several Antibiotics against Escherichia coli Isolates from Australian Cattle Feces Samples, http://repository.ipb.ac.id/handle/123456789/94731, (Accessed: 2.9.2024).

Ansharieta R, Effendi MH, Plumeriastuti H. Genetic Identification of Shiga Toxin Encoding Gene from Cases of Multidrug Resistance (MDR) Escherichia coli Isolated from Raw Milk. Interciencia Journal, (2021); 46 (3): 1-9.

Dsani E, Afari EA, Appiah AD, Kenu E, Kaburi BB, et al. Antimicrobial resistance and molecular detection of extended spectrum Beta-lactamase producing Escherichia coli isolates from raw meat in Greater Accra region, Ghana. BMC Microbiology, (2020); 20: 1–8

Arivo D, Dwiningtyas AW. Antibiotic Sensitivity Test against Escherichia coli Causes Urinary Tract Infections. Journal of Medical Sciences and Health , (2017); 4(4): 216–225.

Wibisono FJ, Sumiarto B, Untari T, Effendi MH, Permatasari DA, et al. Pattern of antibiotic resistance on extended-spectrum beta-lactamases genes producing Escherichia coli on laying hens in Blitar, Indonesia. Biodiversitas, (2020); 21(10): 4631–4635.

Soekoyo AR, Sulistiawati, Wahyu S, Kuntaman K. The Epidemiological Pattern and Risk Factor of ESBL (Extended Spectrum β-Lactamase) Producing Enterobacteriaceae in Gut Bacterial Flora of Dairy Cows and People Surrounding in Rural Area, Indonesia. Indonesian Journal of Tropical and Infectious Disease, (2020); 8(3): 144–151.

Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Research, (2020); 48(D1): D517–D525.

Wibisono FM, Wibisono FJ, Effendi MH, Plumeriastuti H, Hidayatullah AR, et al. A review of salmonellosis on poultry farms: Public health importance. Systematic Reviews in Pharmacy, (2020); 11(9): 481–486.

Permatasari DA, Witaningrum AM, Wibisono FJ, Effendi MH. Detection and prevalence of multidrug-resistant Klebsiella pneumoniae strains isolated from poultry farms in Blitar, Indonesia. Biodiversitas Journal of Biological Diversity, (2020); 21(10): 4642–4647.

Effendi MH, Oktavianto A, Hastutiek P. Tetracycline Resistance Gene In Streptococcus agalactiae Isolated From Bovine Subclinical Mastitis In Surabaya, Indonesia. Jurnal International The Philippine Journal of Veterinary Medicine, (2018); 55(SI): 115–120.




DOI: http://dx.doi.org/10.62940/als.v11i4.1800

Refbacks

  • There are currently no refbacks.