Molecular detection of hlyF gene on multidrug resistance of avian pathogenic Escherichia coli isolated from ducks on wet markets of Surabaya, Indonesia

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IRFAN ALIAS KENDEK
MARIANA FEBRILIANTI RESILINDA PUTRI
FRESHINTA JELLIA WIBISONO
MUSTOFA HELMI EFFENDI
WIWIEK TYASNINGSIH
EMMANUEL NNABUIKE UGBO
NNABUIFE BERNARD AGUMAH

Abstract

Abstract. Kendek IA, Putri MFR, Wibisono FJ, Effendi MH, Tyasningsih W, Ugbo EN, Agumah NB. 2024. Molecular detection of hlyF gene on multidrug resistance of avian pathogenic Escherichia coli isolated from ducks on wet markets of Surabaya, Indonesia. Biodiversitas 25: 1246-1252. Avian Pathogenic Escherichia coli (APEC) is a strain of pathogen that can cause colibacillosis in poultry, including ducks worldwide. This disease can be influenced by various virulence genes, one of which is the hlyF gene which can cause systemic disorders and potentially become zoonotic in poultry. This study aimed to detect the hlyF virulence gene from the multidrug resistance (MDR) properties of Escherichia coli originating from 158 duck cloacal swab samples from seven live markets in Surabaya. Samples were isolated and identified using Eosin Methylene Blue Agar (EMBA) and MacConkey Agar (MCA) media, Gram staining, and then continued with biochemical tests of Triple Sugar Iron Agar (TSIA), Simmons Citrate Agar (SCA), Sulfide Indole Motility (SIM), Methyl red (MR) and Voges-Proskauer (VP). Samples were tested for MDR properties and continued with confirmation of the hlyF virulence gene using PCR. Based on the results of this study, it showed that 85% (134/158) were positive for Escherichia coli. Escherichia coli bacteria experienced resistance to the antibiotic erythromycin 96% (129/134), ciprofloxacin 16% (22/134), antibiotics gentamicin 15% (20/134), aztreonam 4.4% (6/134) and chloramphenicol 3% (5/58). The MDR test results in this study were 15% (20/134), while the PCR test results for the hlyF gene were 60% (12/20). Therefore, Escherichia coli was found to have the hlyF virulence gene, an MDR in Escherichia coli bacteria at the Surabaya live market. Furthermore, APEC strains with the hlyF gene, an MDR, potentially affect public health.

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References
Abd El-Ghany WA. 2023. An Overview on Riemerellosis: A Worldwide Emerging Disease of Ducks. Bulgarian Journal of Veterinary Medicine 26 (3): 309–324. DOI: 10.15547/bjvm.2021-0071.
Abd El-Samie LK, Abd-Elmoaty AM, Ibrahim NA, Darwish WS. 2019. Prevalence and molecular characterization of Avian Pathogenic E. Coli in Ducks. Advances in Animal and Veterinary Sciences 7(2): 163-168. DOI: 10.17582/journal.aavs/2019/7.s2.163.168.
Aberkane C, Messaï A, Messaï CR, Boussaada T. 2023. Antimicrobial resistance pattern of avian pathogenic Escherichia coli with detection of extended-spectrum ?-lactamase-producing isolates in broilers in east Algeria. Veterinary World 16 (3): 449-454. DOI: 10.14202/vetworld.2023.449-454.
Abreu R, Semedo-Lemsaddek T, Cunha E, Tavares L, Oliveira M. 2023. Antimicrobial Drug Resistance in Poultry Production: Current Status and Innovative Strategies for Bacterial Control. Microorganisms 11 (953): 1-35. DOI: 10.3390/microorganisms11040953.
Adrenalin SL, Imanjati LN, Fauziah I, Prakasita VC, Widyarini S, Wahyuni AET. 2020. Virulence Characteristic of Avian Pathogenic Escherichia coli (APEC) Isolates. Jurnal Sain Veteriner 38 (1): 55-60. DOI: 10.22146/jsv.46494.
Afayibo DJA, Zhu H, Zhang B, Yao L, Abdelgawad HA, Tian M, Qi J, Liu Y, Wang S. 2022. Isolation, Molecular Characterization, and Antibiotic Resistance of Avian Pathogenic Escherichia coli in Eastern China. Veterinary Sciences 9 (319): 1-11. DOI: 10.3390/vetsci9070319.
Akanbi OB, Olorunshola ID, Osilojo P, Ademola E, Agada G, Aiyedun J, Odita CI, Ola-Fadunsin SD. 2022. Escherichia Coli Infections, and Antimicrobial Resistance in Poultry Flocks, in North Central Nigeria. Media Kedokteran Hewan 33 (3): 188-207. DOI: 10.20473/mkh.v33i3.2022.188-207.
Allocati N, Masulli M, Alexeyev MF, Di Ilio C. 2013. Escherichia coli in Europe: An overview. International Journal of Environmental Research and Public Health 10: 6235-6254. DOI: 10.3390/ijerph10126235.
Amer MM, Mekky HM, Fedawy HS, El-Shemy A, Bosila MA, Elbayoumi KM. 2020. Molecular identification, genotyping of virulence-associated genes, and pathogenicity of cellulitis-derived Escherichia coli. Veterinary World 13 (12): 2703-2712. DOI: 10.14202/vetworld.2020.2703-2712.
Azam M, Mohsin M, Johnson TJ, Smith EA, Johnson A, Umair M, Saleemi MK, Sajjad-ur-Rahman. 2020. Genomic landscape of multi-drug resistant avian pathogenic Escherichia coli recovered from broilers. Veterinary Microbiology 20 (108766): 1-29. DOI: 10.1016/j.vetmic.2020.108766.
Bakhshi M, Zandi H, Bafghi MF, Astani A, Ranjbar VR, Vakili M. 2020. A survey for phylogenetic relationship; presence of virulence genes and antibiotic resistance patterns of avian pathogenic and uropathogenic Escherichia coli isolated from poultry and humans in Yazd, Iran. Gene Reports 20 (100725): 1–6. DOI: 10.1016/j.genrep.2020.100725.
Banerjee A, Acharyya S. 2021. Prevalence Of Antibiotic Resistance Genes In Indian Ducks:A Comparative Study Between Deshi And Khaki Campbell Ducks. Exploratory Animal and Medical Research 11 (1): 30-37. DOI: 10.52635/EAMR/11.1.30-37.
CLSI. 2020. Performance standards for antimicrobial susceptibility testing. 30th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute.
Dameanti FNAP, Yanestria SM, Widodo A, Effendi MH, Plumeriastuti H, Tyasningsih W, Sutrisno R, Akramsyah MA. 2023. Incidence of Escherichia coli producing Extended-spectrum beta-lactamase (ESBL) in wastewater of dairy farms in East Java, Indonesia. Biodiversitas 24: 1143-1150.
Darwish WS, Eldin WFS, Eldesoky KI. 2015. Prevalence, Molecular Characterization and Antibiotic Susceptibility of Escherichia Coli Isolated from Duck Meat and Giblets. Journal of Food Safety 35 (3): 410-415. DOI: 10.1111/jfs.12189.
Dube N, Mbanga J. 2018. Molecular characterization and antibiotic resistance patterns of avian fecal Escherichia coli from turkeys, geese, and ducks. Veterinary World 11 (6): 859-867. DOI: 10.14202/vetworld.2018.859-867.
Effendi MH, Faridah HD, Wibisono FM, Wibisono FJ, Fatimah, Nisa N, UGBO EN. 2022. Detection of virulence factor encoding genes on Escherichia coli isolated from broiler chicken in Blitar District, Indonesia. Biodiversitas 23 (7): 3429-3436. DOI: 10.13057/biodiv/d230716.
Effendi MH, Tyasningsih W, Yurianti YA, Rahmahani J, Harijani N, Plumeriastuti H. 2021. 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 22 (1): 304-310. DOI: 10.13057/biodiv/d220137.
Eid HM, Algammal AM, Elfeil WK, Youssef FM, Harb SM, Abd-Allah EM. 2019. Prevalence, molecular typing, and antimicrobial resistance of bacterial pathogens isolated from ducks. Veterinary World 12 (5): 677-683. DOI: 10.14202/vetworld.2019.677-683.
Faridah HD, Wibisono FM, Wibisono FJ, Nisa N, Fatimah F, Effendi MH, Ugbo EN, Khairullah AR, Kurniawan SC, Silaen OSM. 2023. Prevalence of the blaCTX-M and blaTEM genes among extended-spectrum beta lactamase–producing Escherichia coli isolated from broiler chickens in Indonesia. J Vet Res. 67 (2023): 179-186
Hardiati A, Safika S, Wibawan IWT, Indrawati A, Pasaribu FH. 2021. Isolation and detection of antibiotics resistance genes of Escherichia coli from broiler farms in Sukabumi, Indonesia. Journal of Advanced Veterinary and Animal Research 8 (1): 84-90. DOI: 10.5455/javar.2021.h489.
Hossain FE, Islam S, Islam MA, Islam S, Ahmed F. 2021. Detection of virulence genes of APEC (avian pathogenic Escherichia coli) isolated from poultry in Noakhali, Bangladesh. Bioresearch Communications 7 (1): 967-972. DOI: 10.3329/brc.v7i1.54253.
Hu J, Afayibo DJA, Zhang B, Zhu H, Yao L, Guo W, Wang X, Wang Z, Wang D, Peng H, Tian M, Qi J, Wang S. 2022. Characteristics, pathogenic mechanism, zoonotic potential, drug resistance, and prevention of avian pathogenic Escherichia coli (APEC). Frontiers in Microbiology 13: 1-13. DOI: 10.3389/fmicb.2022.1049391.
Ievy S, Hoque MN, Islam MS, Sobur MA, Ballah FM, Rahman MS, Rahman MB, Hassan J, Khan MFR, Rahman MT. 2022. Genomic characteristics, virulence, and antimicrobial resistance in avian pathogenic Escherichia coli MTR_BAU02 strain isolated from layer farm in Bangladesh. Journal of Global Antimicrobial Resistance 30: 155-162. DOI: 10.1016/j.jgar.2022.06.001.
Islam MS, Hossain MJ, Sobur MA, Punom SA, Rahman, AMMT, Rahman MT 2023. A Systematic Review on the Occurrence of Antimicrobial-Resistant Escherichia coli in Poultry and Poultry Environments in Bangladesh between 2010 and 2021. BioMed Research International (2425564): 1-18. DOI: 10.1155/2023/2425564.
Januari C, Sudarwanto MB, Purnawarman T. 2019. Antibiotic Resistance In Escherichia coli Isolated From Chicken Meat Of Traditional Markets In The City Of Bogor. Jurnal Veteriner 20 (1): 125-131. DOI: 10.19087/jveteriner.2019.20.1.125.
Jeong J, Lee JY, Kang MS, Lee HJ, Kang SIl, Lee OM, Kwon YK, Kim JH. 2021. Comparative characteristics and zoonotic potential of avian pathogenic Escherichia coli (APEC) isolates from chicken and duck in south korea. Microorganisms 9 (5): 1–17. DOI: 10.3390/microorganisms9050946.
Jiang, F., Huang, X., Barbieri, N. L., Logue, C. M., Nolan, L. K., & Li, G. (2021). Citrate utilization under anaerobic environment in Escherichia coli is under direct control of Fnr and indirect control of ArcA and Fnr via CitA-CitB system. Environmental Microbiology, 23(3), 1496–1509. https://doi.org/10.1111/1462-2920.15357
Johar A, Al-Thani N, Al-Hadidi SH, Dlissi E, Mahmoud MH, Eltai NO. 2021. Antibiotic resistance and virulence gene patterns associated with avian pathogenic Escherichia coli (APEC) from broiler chickens in Qatar. Antibiotics 10 (5): 1-15. DOI: 10.3390/antibiotics10050564.
Kathayat D, Lokesh D, Ranjit S, Rajashekara G. 2021. Avian pathogenic Escherichia coli (APEC): An overview of virulence and pathogenesis factors, zoonotic potential, and control strategies. Pathogens 10 (4), 1-32. DOI: 10.3390/pathogens10040467.
Kika TS, Cocoli S, Peli? DL, Puva?a N, Lika E, Peli? M. 2023. Colibacillosis in Modern Poultry Production. Journal of Agronomy, Technology and Engineering Management 6 (6): 975-987. DOI: 10.55817/yzfa3391.
Kissinga HD, Mwombeki F, Said K, Katakweba AAS, Nonga HE, Muhairwa AP. 2018. Antibiotic susceptibilities of indicator bacteria Escherichia coli and Enterococci spp. isolated from ducks in Morogoro Municipality, Tanzania. BMC Research Notes 11 (87): 1-6. DOI: 10.1186/s13104-018-3201-4.
Li G, Li X, Hu J, Pan Y, Ma Z, Zhang L, Xiong W, Zeng D, Zeng Z. 2023. Molecular epidemiology and transmission of rmtB-positive Escherichia coli among ducks and environment. Poultry Science 102: 102579. DOI: 10.1016/j.psj.2023.102579.
Li R, Li N, Zhang J, Wang Y, Liu J, Cai Y, Chai T, Wei L. 2016. Expression of immune-related genes of ducks infected with avian pathogenic Escherichia coli (APEC). Frontiers in Microbiology 7 (637): 1-9. DOI: 10.3389/fmicb.2016.00637.
Logue CM, Wannemuehler Y, Nicholson BA, Doetkott C, Barbieri NL, Nolan LK. 2017. Comparative analysis of phylogenetic assignment of human and avian ExPEC and fecal commensal Escherichia coli using the (previous and revised) clermont phylogenetic typing methods and its impact on avian pathogenic Escherichia coli (APEC) classification. Frontiers in Microbiology 8 (283): 1-11. DOI: 10.3389/fmicb.2017.00283.
Maciel JF, Matter LB, Trindade MM, Camillo G, Lovato M, Botton SDA, de Vargas AC. 2017. Virulence factors and antimicrobial susceptibility profile of extraintestinal Escherichia coli isolated from an avian colisepticemia outbreak. Microbial Pathogenesis 103: 119-122. DOI: 10.1016/j.micpath.2016.12.020
Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. 2018. Antibiotic use in agriculture and its consequential resistance in environmental sources: Potential public health implications. In Molecules 23 (795): 1-48. DOI: 10.3390/molecules23040795.
Murase K, Martin P, Porcheron G, Houle S, Helloin E, Pénary M, Nougayrède JP, Dozois CM, Hayashi T, Oswald E. 2015. HlyF produced by extraintestinal pathogenic Escherichia coli is a virulence factor that regulates outer membrane vesicle biogenesis. Journal of Infectious Diseases 213: 856-865. DOI: 10.1093/infdis/jiv506.
Musa L, Proietti PC, Branciari R, Menchetti L, Bellucci S, Ranucci D, Marenzoni ML, Franciosin MP. 2020. Antimicrobial Susceptibility of Escherichia coli and ESBL-Producing Escherichia coli Diffusion in Conventional, Organic and Antibiotic-Free Meat Chickens at Slaughter. Animals Mdpi 10: 1-12. DOI: 10.3390/Ani10071215.
Na SH, Moon DC, Choi MJ, Oh SJ, Jung DY, Sung EJ, Kang HY, Hyun BH, Lim SK. 2019. Antimicrobial Resistance and Molecular Characterization of Extended-Spectrum ?-Lactamase-Producing Escherichia coli Isolated from Ducks in South Korea. Foodborne Pathogens and Disease 20 (20): 1-8. DOI: 10.1089/fpd.2019.2644.
Newman DM, Barbieri NL, de Oliveira AL, Willis D, Nolan LK, Logue CM. 2021. Characterizing avian pathogenic Escherichia coli (APEC) from colibacillosis cases, 2018. PeerJ 9 (11025): 1-24. DOI: 10.7717/peerj.11025.
Oliveira ES, Cardozo MV, Borzi MM, Borges CA, Guastalli EAL, Ávila FA. 2019. Highly pathogenic and multidrug resistant avian pathogenic Escherichia coli in free-range chickens from Brazil. Brazilian Journal of Poultry Science 21 (1): 1-8. DOI: 10.1590/1806-9061-2018-0876.
Ovi F, Zhang L, Nabors H, Jia L, Adhikari P. 2023. A compilation of virulence-associated genes that are frequently reported in avian pathogenic Escherichia coli (APEC) compared to other Escherichia coli. Journal of Applied Microbiology 134 (3): 1-20. DOI: 10.1093/jambio/lxad014.
Papouskova A, Masarikova M, Valcek A, Senk D, Cejkova D, Jahodarova E, Cizek A. 2020. Genomic analysis of Escherichia coli strains isolated from diseased chicken in the Czech Republic. BMC Veterinary Research 16 (1): 1-10. DOI: 10.1186/s12917-020-02407-2.
Prayudi SKA, Effendi MH, Lukiswanto BS, Az Zah-Ra RL, Benjamin MI, Kurniawan SC, Khairullah AR, Silaen OSM, Lisnanti EF, Baihaqi ZA, Widodo A, Riwu KHP. 2023. Detection of Genes on Escherichia coli Producing Extended Spectrum ?-lactamase Isolated from the Small Intestine of Ducks in Traditional Markets Surabaya City, Indonesia. Journal of Advanced Veterinary Research 13 (8): 1600–1608.
Putri MFR, Kendek IA, Wibisono FJ, Effendi MH, Rahardjo D, Tyasningsih W, Ugbo EN. 2023. Molecular detection of iron gene on multidrug resistant avian fecal Escherichia coli isolated from broiler on traditional markets, Surabaya , Indonesia. Biodiversitas 24 (12): 6454–6460. DOI: 10.13057/biodiv/d241207.
Rahmahani J, Salamah, Mufasirin, Tyasningsih W, Effendi MH. 2020. Antimicrobial resistance profile of Escherichia coli from cloacal swab of domestic chicken in Surabaya traditional market. Biochemical and Cellular Archives 20 (1): 2993–2997. DOI: 10.35124/bca.2020.20.S1.2993.
Ramaditya NA, Besung INK, Mahardika IGNK. 2019. Detection and Sequencing Genes Iron, Iuta, and Hlyf in Avian Pathogenic Eschericia coli. Buletin Veteriner Udayana 11 (2): 229-238. DOI: 10.24843/bulvet.2019.v11.i02.p16.
Saha O, Hoque MN, Islam OK, Rahaman MM, Sultana M, Hossain MA. 2020. Multidrug-resistant avian pathogenic Escherichia coli strains and association of their virulence genes in Bangladesh. Microorganisms 8 (1135): 1–23. DOI: 10.3390/microorganisms8081135.
Samuel M, Wabwire TF, Tumwine G, Waiswa P. 2023. Antimicrobial Usage by Small-Scale Commercial Poultry Farmers in Mid-Western District of Masindi Uganda: Patterns, Public Health Implications, and Antimicrobial Resistance of Eschericia coli. Veterinary Medicine International (6644271): 1-10. DOI: 10.1155/2023/6644271.
Sarker MS, Kabir ME, Mahua FA, Ahmed A, Ripon RK, Silva V, Poeta P, Ahad A. 2022. Antibiotic-Resistant Escherichia coli Isolated from Duck Cloacal and Tap Water Samples at Live Bird Markets in Bangladesh. Poultry Science Journal 11 (1): 19-27. DOI: 10.22069/psj.2022.20028.1789.
Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugla-Ploskonska G, Choroszy-Krol I. 2019. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports. Gut Pathogens 11 (10): 1-16. DOI: 10.1186/s13099-019-0290-0.
Sgariglia E, Mandolini NA, Napoleoni M, Medici L, Fraticelli R, Conquista M, Gianfelici P, Staffolani M, Fisichella S, Capuccella M, Sargenti M, Perugini G. 2019. Antibiotic resistance pattern and virulence genes in avian pathogenic Escherichia coli (APEC) from different breeding systems. Veterinaria Italiana, 55(1), 27–33. https://doi.org/10.12834/VetIt.1617.8701.1.
Singh A, Khan MSR., Saha S, Hassan J, Roy U. 2012. Isolation and Detection of Antibiotic Sensitivity Pattern of Escherichia coli from Ducks in Bangladesh and Nepal. Microbes and Health 1 (1): 6-8. DOI: 10.3329/mh.v1i1.13704.
Soman M, Nair SR, Mini M, Mani BK, Joseph S, Department. 2014. Isolation and polymerase chain reaction-based identification of Riemerella anatipestifer from ducks in Kerala, India. Veterinary World 7 (9): 765-769. DOI: 10.14202/vetworld.2014.765-769.
Sora VM, Meroni G, Martino PA, Soggiu A, Bonizzi L, Zecconi A. 2021. Extraintestinal pathogenic Escherichia coli: Virulence factors and antibiotic resistance. Pathogens 10 (1355): 1-25. DOI: 10.3390/pathogens10111355
Subedi M, Bhattarai RK, Devkota B, Phuyal S, Luitel H. 2018. Correction: Antibiotic resistance pattern and virulence genes content in avian pathogenic Escherichia coli (APEC) from broiler chickens in chitwan, Nepal. BMC Veterinary Research 14 (113): 1-6. DOI: 10.1186/s12917-018-1442-z.
Tyasningsih W, Ramandinianto SC, Ansharieta R, Witaningrum AM, Permatasari DA, Wardhana DK, Effendi MH, Ugbo EN. 2022. Prevalence and antibiotic resistance of Staphylococcus aureus and Escherichia coli isolated from raw milk in East Java, Indonesia. Veterinary World 15 (8): 2021-2028. DOI: 10.14202/vetworld.2022.2021-2028.
Velhner M, Suvajdži? L, Todorovi? D, Milanov D, Kozoderovi? G. 2018. Avian pathogenic Escherichia coli: diagnosis, virulence and prevention. Archives of Veterinary Medicine 11 (2): 21-31. DOI: 10.46784/e-avm.v11i2.23.
Vidovic N, Vidovic S. 2020. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics 9 (52): 1–15. DOI: 10.3390/antibiotics9020052.
Vivijs B, Moons P, Aertsen A, Michiels CW. 2014. Acetoin synthesis acquisition favors Escherichia coli growth at low pH. Applied and Environmental Microbiology 80 (19): 6054-6061. DOI: 10.1128/AEM.01711-14.
Wall S. 2019. Prevention of antibiotic resistance–an epidemiological scoping review to identify research categories and knowledge gaps. Global Health Action 12 (1756191): 1-28. DOI: 10.1080/16549716.2020.1756191.
Wang Z, Xu S, Zheng X, Zheng X, Liu M, Guo G, Yu Y, Han X, Liu Y, Wang K, Zhang W. 2023. Identification of Subunits for Novel Universal Vaccines against Three Predominant Serogroups and the Emerging O145 among Avian Pathogenic Escherichia coli by Pan-RV Pipeline. Applied and Environmental Microbiology, 89 (1): 1–15. DOI: 10.1128/aem.01061-22.
Wei B, Cha SY, Kang M, Park IJ, Moon OK, Park CK, Jang HK. 2013. Development and application of a multiplex PCR assay for rapid detection of 4 major bacterial pathogens in ducks. Poultry Science 92 (5): 1164–1170. DOI: 10.3382/ps.2012-02823.
Wibisono FJ, Sumiarto B, Untari T, Effendi MH, Permatasari DA, Witaningrum AM. 2020. CTX Gene of Extended Spectrum Beta-Lactamase (ESBL) Producing Escherichia coli on Broilers in Blitar, Indonesia. Systematic Reviews in Pharmacy 11 (7): 396-403. DOI: 10.31838/srp.2020.7.59.
Wibisono FJ, Sumiarto B, Untari T, Effendi MH, Permatasari DA, Witaningrum AM. 2021. Molecular identification of ctx gene of extended spectrum betalactamases (ESBL) producing Escherichia coli on layer chicken in blitar, indonesia. Journal of Animal and Plant Sciences 31 (4): 954–959. DOI: 10.36899/JAPS.2021.4.0289.
Xu X, Sun Q, Zhao L. 2019. Virulence factors and antibiotic resistance of avian pathogenic Escherichia coli in eastern China. Journal of Veterinary Research (Poland) 63 (3): 317-320. DOI: 10.2478/jvetres-2019-0056.
Yanestria SM, Dameanti FNAEP, Musayannah BG, Pratama JWA, Witaningrum AM, Effendi, MH, Ugbo EN. 2022. Antibiotic resistance pattern of Extended-Spectrum ?-Lactamase (ESBL) producing Escherichia coli isolated from broiler farm environment in Pasuruan district, Indonesia. Biodiversitas 23 (9): 4460-4465. DOI: 10.13057/biodiv/d230911.
Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, Han X, Qiu H, Price S, Cheng D, Wang C. 2017. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PLoS ONE 12 (9): 1-8. DOI: 10.1371/journal.pone.0185326.
Yousef HMY, Hashad ME, Osman KM, Alatfeehy NM, Hassan WMM, Elebeedy LA, Salem HM, Shami A, Al-Saeed FA, El-Saadony MT, El-Tarabily KA, Marouf S. 2023. Surveillance of Escherichia coli in different types of chicken and duck hatcheries: one health outlook. Poultry Science 102 (12): 103108. DOI: 10.1016/j.psj.2023.103108.
Zhang S, Shu Y, Wang Y, Zhong Z, Wang M, Jia R, Chen S, Liu M, Zhu D, Zhao X, Wu Y, Yang Q, Huang J, Ou X, Mao S, Gao Q, Sun D, Tian B, Cheng A. 2023. High rate of multidrug resistance and integrons in Escherichia coli isolates from diseased ducks in select regions of China. Poultry Science 102 (10): 1–13.DOI: 10.1016/j.psj.2023.102956.

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