Detection of ESBL-Encoding Genes in Antibiotic-Resistant Escherichia coli Isolated  from Houseflies (Musca domestica) in Campus Food Court

Denny Widaya Lukman; Herwin Pisestyani; Muhammad Rizki Aminudin; Supriyono Supriyono; Eddy Sukmawinata

doi:10.22146/jsv.105866

Detection of ESBL-Encoding Genes in Antibiotic-Resistant Escherichia coli Isolated from Houseflies (Musca domestica) in Campus Food Court

https://doi.org/10.22146/jsv.105866

Denny Widaya Lukman^(1*), Herwin Pisestyani⁽²⁾, Muhammad Rizki Aminudin⁽³⁾, Supriyono Supriyono⁽⁴⁾, Eddy Sukmawinata⁽⁵⁾

(1) School of Veterinary Medicine and Biomedical Sciences, IPB University
(2) School of Veterinary Medicine and Biomedical Sciences, IPB University
(3) School of Veterinary Medicine and Biomedical Sciences, IPB University
(4) School of Veterinary Medicine and Biomedical Sciences, IPB University
(5) National Research and Innovation Agency
(*) Corresponding Author

Abstract

Escherichia coli is a dangerous pathogen that is reported to bring about disease in humans as well as animals. E. coli is commonly associated with diseases due to food contamination. Some strains of the pathogen have shown resistance to various antibiotics, one of them is ESBL-E. coli, leading to complex problems in health. The transmission of pathogenic bacteria in the environment can be mediated by houseflies (Musca domestica). This study aimed to analyze the presence of antibiotic-resistant E. coli bacteria and detect resistance genes carried by houseflies (M. domestica) collected from food courts in IPB University, Dramaga Bogor, Indonesia. The study included isolation and identification of E. coli bacteria based on ISO 16649-2: 2001 standards. E. coliisolates are then tested for antibiotic sensitivity using the Kirby Bauer disc diffusion method based on CLSI in 2023. Antibiotics tested included ciprofloxacin, ampicillin, tetracycline, trimethoprim-sulfamethoxazole, chloramphenicol, ceftazidime, and cefotaxime. Then, the identification of genes encoding ESBL resistance (blaCTX, blaTEM, and blaSHV) was conducted. The study found 5 isolates (5/40; 12.5%). Total 4 isolates of 5 isolates indicated resistance against two or several antibiotics tested. Detection of genes encoding ESBL resistance in 5 E. coli isolates showed that 2 isolates (40%) were positive for the blaTEM gene but did not show positive results for blaCTX and blaSHV genes. The appearance of antibiotic-resistant E. coli in houseflies in food court in campus should be taken into account.

Keywords

Antibiotic resistance; ESBL; MDR; Musca domestica; vector

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References

Akter, S., Sabuj, A. A. M., Haque, Z. F., Rahman, M. T., Kafi, M. A., & Saha, S. (2020). Detection of antibiotic-resistant bacteria and their resistance genes from houseflies. Veterinary World, 13(2), 266–274. https://doi.org/10.14202/vetworld.2020.266-274 Ansharieta, R., Ramandinianto, S. C., Effendi, M. H., & Plumeriastuti, H. (2021). Molecular identification of blaCTX-M and blaTEM genes encoding extended-spectrum ß-lactamase (ESBL) producing Escherichia coli isolated from raw cow’s milk in East Java, Indonesia. Biodiversitas Journal of Biological Diversity, 22(4), 1600–1605. https://doi.org/10.13057/biodiv/d220402 Asari, K. A., Lukman, D. W., & Purnawarman, T. (2021). Identifikasi Escherichia coli yang Resistan Antibiotik pada Daging Burger yang Dijual di Sekitar Kampus IPB Dramaga Bogor. Jurnal Veteriner, 22(4), 515–522. https://doi.org/10.19087/jveteriner.2021.22.4.515 Aulia, S. A., Sutiningsih, D., Setyawan, H., & Udiyono, A. (2023). Keberadaan Residu Tetrasiklin pada Daging Ayam Broiler di Kabupaten Kudus (Studi di Pasar Tradisional dan Pasar Modern Tahun 2019). Jurnal Epidemiologi Kesehatan Komunitas, 8(1), 69–75. https://doi.org/10.14710/jekk.v8i1.6918 Autmizguine, J., Melloni, C., Hornik, C. P., Dallefeld, S., Harper, B., Yogev, R., Sullivan, J. E., Atz, A. M., Al-Uzri, A., Mendley, S., Poindexter, B., Mitchell, J., Lewandowski, A., Delmore, P., Cohen-Wolkowiez, M., & Gonzalez, D. (2018). Population Pharmacokinetics of Trimethoprim-Sulfamethoxazole in Infants and Children. Antimicrobial Agents and Chemotherapy, 62(1), 1–19. https://doi.org/10.1128/AAC.01813-17 CDC. (2019). Antibiotic resistance threats in the United States, 2019. https://doi.org/10.15620/cdc:82532 CLSI. (2023). Performance standards for antimicrobial susceptibility testing (30th Edition, p. 282). Clinical and Laboratory Standards Institute. Effendi, M. H., Hartadi, E. B., Witaningrum, A. M., Permatasari, D. A., & Ugbo, E. N. (2022). Molecular identification of blaTEM gene of extended-spectrum beta-lactamase-producing Escherichia coli from healthy pigs in Malang district, East Java, Indonesia. Journal of Advanced Veterinary and Animal Research, 9(3), 447–452. https://doi.org/10.5455/javar.2022.i613 Efstratiou, M. A., Bountouni, M., & Kefalas, E. (2018). Spread of Antibiotic Resistance in Aquatic Environments: E. coli as a Case Study. EWaS3 2018, 693. https://doi.org/10.3390/proceedings2110693 Faridah, H. D., Wibisono, F. M., Wibisono, F. J., Nisa, N., Fatimah, F., Effendi, M. H., Ugbo, E. N., Khairullah, A. R., Kurniawan, S. C., & Silaen, O. S. M. (2023). Prevalence of the blaCTX-M and blaTEM genes among extended-spectrum beta lactamase–producing Escherichia coli isolated from broiler chickens in Indonesia. Journal of Veterinary Research, 67(2), 179–186. https://doi.org/10.2478/jvetres-2023-0025 Geden, C. J., Nayduch, D., Scott, J. G., Burgess, E. R., Gerry, A. C., Kaufman, P. E., Thomson, J., Pickens, V., & Machtinger, E. T. (2021). House Fly (Diptera: Muscidae): Biology, Pest Status, Current Management Prospects, and Research Needs. Journal of Integrated Pest Management, 12(1). https://doi.org/10.1093/jipm/pmaa021 Gundran, R. S., Cardenio, P. A., Villanueva, M. A., Sison, F. B., Benigno, C. C., Kreausukon, K., Pichpol, D., & Punyapornwithaya, V. (2019). Prevalence and distribution of blaCTX-M, blaSHV, blaTEM genes in extended- spectrum β- lactamase- producing E. coli isolates from broiler farms in the Philippines. BMC Veterinary Research, 15(277), 1–8. https://doi.org/10.1186/s12917-019-1975-9 Halawani, E. M., Hassan, A. M., & Gad El-Rab, S. M. (2020). Nanoformulation of Biogenic Cefotaxime-Conjugated-Silver Nanoparticles for Enhanced Antibacterial Efficacy Against Multidrug-Resistant Bacteria and Anticancer Studies. International Journal of Nanomedicine, Volume 15, 1889–1901. https://doi.org/10.2147/IJN.S236182 Isam-Eldeen, I. I. B., AlaaEldin, Y. M. H., Mohamed, A. I. H., & Eltayib, H. A.-A. (2022). Isolation of potentially pathogenic bacteria from Musca domestica captured in hospitals and slaughterhouses, Khartoum state, Sudan. African Journal of Microbiology Research, 16(2), 76–81. https://doi.org/10.5897/ajmr2021.9580 Islam, Md. S., Sobur, Md. A., Rahman, S., Ballah, F. M., Ievy, S., Siddique, M. P., Rahman, M., Kafi, Md. A., & Rahman, Md. T. (2022). Detection of blaTEM, blaCTX-M, blaCMY, and blaSHV Genes Among Extended-Spectrum Beta-Lactamase-Producing Escherichia coli Isolated from Migratory Birds Travelling to Bangladesh. Microbial Ecology, 83(4), 942–950. https://doi.org/10.1007/s00248-021-01803-x Lindeberg, Y. L., Egedal, K., Hossain, Z. Z., Phelps, M., Tulsiani, S., Farhana, I., Begum, A., & Jensen, P. K. M. (2018). Can Escherichia coli fly? The role of flies as transmitters of E. coli to food in an urban slum in Bangladesh. Tropical Medicine and International Health, 23(1), 2–9. https://doi.org/10.1111/tmi.13003 Matesanz, M., & Mensa, J. (2021). Ceftazidime-avibactam. Revista Española de Quimioterapia, 34(Suppl 1), 38–40. https://doi.org/10.37201/req/s01.11.2021 Mustika, Y. R., Effendi, M. H., Puspitasari, Y., Plumeriastuti, H., Khairullah, A. R., & Kinasih, K. N. (2024). Identification of Escherichia coli Multidrug Resistance in Cattle in Abattoirs. Jurnal Medik Veteriner, 7(1), 19–32. https://doi.org/10.20473/jmv.vol7.iss1.2024.19-32 Nihei, S. S., & De Carvalho, C. J. B. (2009). The Muscini flies of the world (Diptera, Muscidae): identification key and generic diagnoses. Zootaxa, 1976(1). https://doi.org/10.11646/zootaxa.1976.1.1 Nishino, K., Yamasaki, S., Nakashima, R., Zwama, M., & Hayashi-Nishino, M. (2021). Function and Inhibitory Mechanisms of Multidrug Efflux Pumps. Frontiers in Microbiology, 12. https://doi.org/10.3389/fmicb.2021.737288 O’Neill, J. (2016). Tackling drug-resistant infections globally: final report and recommendations the review on antimicrobial resistance chaired by Jim O’neill. https://apo.org.au/node/63983 Onwugamba, F. C., Mellmann, A., Nwaugo, V. O., Süselbeck, B., & Schaumburg, F. (2020). Antimicrobial resistant and enteropathogenic bacteria in ‘filth flies’: a cross-sectional study from Nigeria. Scientific Reports, 10(1), 16990. https://doi.org/10.1038/s41598-020-74112-x Punyadi, P., Thongngen, P., Kiddee, A., Assawatheptawee, K., Tansawai, U., Bunchu, N., & Niumsup, P. R. (2021). Prevalence of blaCTX-M and Emergence of blaCTX-M-5 Carrying Escherichia coli in Chrysomya megacephala (Diptera: Calliphoridae), Northern Thailand. Microbial Drug Resistance, 27(5), 698–705. https://doi.org/10.1089/mdr.2020.0249 Putra, J. K., Wahyuni, A. E. T. H., & Untari, T. (2024). Sensitivitas Escherichia coli yang diisolasi dari unggas Phasianidae terhadap berbagai jenis antibiotika. Resiliensi Industri Peternakan Tropis, 247–262. Rahman, M. M., Husna, A., Elshabrawy, H. A., Alam, J., Runa, N. Y., Badruzzaman, A. T. M., Banu, N. A., Al Mamun, M., Paul, B., Das, S., Rahman, Md. M., Mahbub-E-Elahi, A. T. M., Khairalla, A. S., & Ashour, H. M. (2020). Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Scientific Reports, 10(1), 1–11. https://doi.org/10.1038/s41598-020-78367-2 Sari, D. Y., Pisestyani, H., & Lukman, D. W. (2020). Antibiotic resistance in Escherichia coli isolated from doner kebab sold in dramaga bogor, Indonesia. Advances in Animal and Veterinary Sciences, 8(3), 278–284. https://doi.org/10.17582/journal.aavs/2020/8.3.278.284 Saujana, R. A. (2023). Resistansi Isolat Escherichia coli dari Daging Ayam Suwir Bubur Ayam yang Dijual di Lingkar Kampus Institut Pertanian Bogor. Sekolah Kedokteran Hewan dan Biomedis IPB University, Bogor. Sobur, A., Haque, Z. F., Sabuj, A. A. M., Ievy, S., Rahman, A. M. M. T., El Zowalaty, M. E., & Rahman, T. (2019). Molecular Detection of Multidrug and Colistin-Resistant Escherichia coli isolated from house flies in various environmental settings. Future Microbiology, 14(10), 847–858. https://doi.org/10.2217/fmb-2019-0053 Soufiane, S. D. M., Serge, Y. R., Tinlé, B., Sévérin, N., Firmin, K. N., Isidore, T., Jacques, Z., Inès, Y., Félicité, N., Aminata, F., Naomi, B., Jean-Bosco, O., Ibrahim, S., & Mahamoudou, S. (2024). Detection and molecular characterization of multiresistant Enterobacteriaceae carried by houseflies in the city of Bobo-Dioulasso, Burkina Faso. International Journal of One Health, 10(1), 12–19. https://doi.org/10.14202/IJOH.2024.12-19 Suhartono, S., Hayati, Z., & Hayatunnida, R. (2023). Distribution of Multidrug Resistant Escherichia coli and Klebsiella pneumoniae Isolates among clinical specimens in the Zainoel Abidin General Hospital, Banda Aceh, Indonesia. Research Journal of Pharmacy and Technology, 16(6), 2854–2858. https://doi.org/10.52711/0974-360X.2023.00470 Sumampouw, O. J. (2018). Uji Sensitivitas Antibiotik terhadap Bakteri Escherichia coli Penyebab Diare Balita di Kota Manado . Journal of Current Pharmaceutical Sciences, 2(1)(2598–2095), 104–110. Syafriana, V., Hamida, F., Sukamto, A. R., & Aliya, L. S. (2020). Resistensi Escherichia coli dari Air Danau ISTN Jakarta Terhadap Antibiotik Amoksisilin, Tetrasiklin, Kloramfenikol, dan Siprofloksasin. Sainstech Farma, 13(3), 92–98. https://doi.org/doi.org/10.37277/sfj.v13i2.761 Tolenada, C. P. S., & Dayrit, G. B. (2023). Presence of blaCTXM-1, blaCTXM-9, and blaTEM-1 Genes in Extended-spectrum β-lactamase-producing Escherichia coli Isolates from Hospital Wastewater. The Indonesian Biomedical Journal, 15(5), 278–287. https://doi.org/10.18585/inabj.v15i5.2531 WHO. (2020). Vector-borne diseases. https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases Wibisono, F. J., Sumiarto, B., Untari, T., Effendi, M. H., Permatasari, D. A., & Witaningrum, A. M. (2020). Prevalensi dan Analisis Faktor Risiko Multidrug Resistance Bakteri Escherichia coli pada Ayam Komersial di Kabupaten Blitar. Jurnal Ilmu Peternakan Dan Veteriner Tropis, 10(1), 15–22. https://doi.org/10.46549/jipvet.v10i1.74 Wibisono, F. M., Faridah, H. D., Wibisono, F. J., Tyasningsih, W., Effendi, M. H., Witaningrum, A. M., & Ugbo, E. N. (2021). Detection of invA virulence gene of multidrug-resistant Salmonella species isolated from the cloacal swab of broiler chickens in Blitar district, East Java, Indonesia. Veterinary World, 14(12), 3126–3131. https://doi.org/10.14202/vetworld.2021.3126-3131 Widodo, A., Lamid, M., Effendi, M. H., Tyasningsih, W., Raharjo, D., Khairullah, A. R., Kurniawan, S. C., Yustinasari, L. R., Riwu, K. H. P., & Silaen, O. S. M. (2023). Molecular identification of blaTEM and blaCTX-M genes in multidrug-resistant Escherichia coli found in milk samples from dairy cattle farms in Tulungagung, Indonesia. Journal of Veterinary Research, 67(3), 381–388. https://doi.org/10.2478/jvetres-2023-0052 Woodford, N., Fagan, E. J., & Ellington, M. J. (2006). Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. Journal of Antimicrobial Chemotherapy, 57(1), 154–155. https://doi.org/10.1093/jac/dki412 Yin, J. H., Kelly, P. J., & Wang, C. (2022). Flies as Vectors and Potential Sentinels for Bacterial Pathogens and Antimicrobial Resistance: A Review. Veterinary Sciences, 9(300), 1–10. https://doi.org/10.3390/vetsci9060300 Zhang, G.-F., Liu, X., Zhang, S., Pan, B., & Liu, M.-L. (2018). Ciprofloxacin derivatives and their antibacterial activities. European Journal of Medicinal Chemistry, 146, 599–612. https://doi.org/10.1016/j.ejmech.2018.01.078

DOI: https://doi.org/10.22146/jsv.105866