Prevalence of Antimicrobial Resistance in Escherichia coli and Salmonella Species Isolates from Chickens in Live Bird Markets and Boot Swabs from Layer Farms in Timor-Leste
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area and Population
2.2. Data Collection from Live Bird Markets
2.3. Data Collection from Layer Farms
2.4. Isolation and Identification of Bacteria
2.5. Antimicrobial Susceptibility Testing
2.6. Data Analysis
3. Results
3.1. Origin of Samples and Recovery of Isolates
3.2. Disk Diffusion Results
3.3. Broth-Based Microdilution Results
3.4. Comparison of Antimicrobial Resistance in Different Chicken Populations
4. Discussion
4.1. Strength of the Study and Key Findings
4.2. Recovery Rate of Isolates
4.3. Antimicrobial Resistance in Different Chicken Populations
4.4. Public Health Implications
4.5. Origin of Samples
4.6. Capacity Building and One Health
4.7. Future Work
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ventola, C.L. The antibiotic resistance crisis: Part 1: Causes and threats. Pharm. Ther. 2015, 40, 277–283. [Google Scholar]
- Mulchandani, R.; Wang, Y.; Gilbert, M.; Van Boeckel, T.P. Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLoS Glob. Public Health 2023, 3, e0001305. [Google Scholar] [CrossRef]
- Morel, C.M.; Alm, R.A.; Årdal, C.; Bandera, A.; Bruno, G.M.; Carrara, E.; Colombo, G.L.; de Kraker, M.E.A.; Essack, S.; Frost, I.; et al. A one health framework to estimate the cost of antimicrobial resistance. Antimicrob. Resist. Infect. Control 2020, 9, 187. [Google Scholar] [CrossRef]
- O’Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations; Government of the United Kingdom: London, UK, 2016.
- Laxminarayan, R.; Duse, A.; Wattal, C.; Zaidi, A.K.M.; Wertheim, H.F.L.; Sumpradit, N.; Vlieghe, E.; Hara, G.L.; Gould, I.M.; Goossens, H.; et al. Antibiotic resistance—The need for global solutions. Lancet Infect. Dis. 2013, 13, 1057–1098. [Google Scholar] [CrossRef]
- General Directorate of Statistics—Ministry of Finance (Timor Leste). Timor-Leste Population and Housing Census 2022—Preliminary Results. Available online: https://timor-leste.unfpa.org/sites/default/files/pub-pdf/censuspreliminaryresults2022_4.pdf (accessed on 12 December 2023).
- Bettencourt, E.; Tilman, M.; Narciso, V.; Da Silva Carvalho, M.L.; Henriques, P. The Livestock Roles in the Wellbeing of Rural Communities of Timor-Leste. Rev. Econ. Sociol. Rural. 2015, 53, 63–80. [Google Scholar] [CrossRef]
- General Directorate of Statistics—Ministry of Finance (Timor Leste); Ministry of Agriculture and Fisheries. Timor-Leste Agriculture Census 2019: National Report on Final Census Results. Available online: https://inetl-ip.gov.tl/2023/03/16/2241/ (accessed on 12 December 2023).
- Lundahl, M.; Sjöholm, F. Improving the lot of the farmer: Development challenges in Timor-Leste during the second decade of independence. Asian Econ. Pap. 2013, 12, 71–96. [Google Scholar] [CrossRef]
- Wong, J.T.; Bagnol, B.; Grieve, H.; da Costa Jong, J.B.; Li, M.; Alders, R.G. Factors influencing animal-source food consumption in Timor-Leste. Food Secur. 2018, 10, 741–762. [Google Scholar] [CrossRef]
- World Food Programme. Fill the Nutrient Gap—Timor-Leste. Available online: https://www.wfp.org/publications/fill-nutrient-gap-timor-leste (accessed on 12 December 2023).
- Smith, D.; Cooper, T. Evaluating the Opportunities for Smallholder Livestock Keepers in Timor-Leste. Available online: https://www.aciar.gov.au/sites/default/files/2021-12/LS-2017-035-final-report.pdf (accessed on 20 September 2022).
- Da Cruz, C.J. Livestock Development in East Timor. Available online: https://www.aciar.gov.au/sites/default/files/legacy/node/512/pr113.pdf#page=16 (accessed on 12 December 2023).
- Ting, S.; Pereira, A.; Alves, A.d.J.; Fernandes, S.; Soares, C.d.C.; Soares, F.J.; Henrique, O.d.C.; Davis, S.; Yan, J.; Francis, J.R.; et al. Antimicrobial use in animals in Timor-Leste based on veterinary antimicrobial imports between 2016 and 2019. Antibiotics 2021, 10, 426. [Google Scholar] [CrossRef]
- Mottet, A.; Tempio, G. Global poultry production: Current state and future outlook and challenges. World’s Poult. Sci. J. 2017, 73, 245–256. [Google Scholar] [CrossRef]
- Ting, S.; Pereira, A.; Alves, A.; Vong da Silva, P.G.; Dos Santos, C.; Davis, S.; Sidjabat, H.E.; Yan, J.; Francis, J.R.; Bendita da Costa Jong, J.; et al. Knowledge, attitudes and practices of government animal health workers on antibiotic use and antibiotic resistance in Timor-Leste. Front. Vet. Sci. 2022, 9, 1063530. [Google Scholar] [CrossRef]
- Ting, S.; Pereira, A.; Davis, S.; Vong da Silva, P.G.; Alves, A.; Dos Santos, C.; Toribio, J.-A.L.M.L.; Morais, O.; da Costa Jong, J.B.; Barnes, T.S. Knowledge and practices on antibiotic use and antibiotic resistance among smallholder pig farmers in Timor-Leste. Front. Vet. Sci. 2022, 8, 819643. [Google Scholar] [CrossRef]
- Food and Agriculture Organisation. Monitoring and Surveillance of Antimicrobial Resistance in Bacteria from Healthy Food Animals Intended for Consumption. Available online: https://www.fao.org/documents/card/en?details=ca6897en/ (accessed on 10 December 2023).
- de Mesquita Souza Saraiva, M.; Lim, K.; do Monte, D.F.M.; Givisiez, P.E.N.; Alves, L.B.R.; de Freitas Neto, O.C.; Kariuki, S.; Júnior, A.B.; de Oliveira, C.J.B.; Gebreyes, W.A. Antimicrobial resistance in the globalized food chain: A One Health perspective applied to the poultry industry. Braz. J. Microbiol. 2022, 53, 465–486. [Google Scholar] [CrossRef]
- Van Boeckel, T.P.; Pires, J.; Silvester, R.; Zhao, C.; Song, J.; Criscuolo, N.G.; Gilbert, M.; Bonhoeffer, S.; Laxminarayan, R. Global trends in antimicrobial resistance in animals in low- and middle-income countries. Science 2019, 365, eaaw1944. [Google Scholar] [CrossRef] [PubMed]
- Riley, L.W. Distinguishing Pathovars from Nonpathovars: Escherichia coli. Microbiol. Spectr. 2020, 8, AME-0014-2020. [Google Scholar] [CrossRef]
- Parvej, M.S.; Nazir, K.H.; Rahman, M.B.; Jahan, M.; Khan, M.F.; Rahman, M. Prevalence and characterization of multi-drug resistant Salmonella Enterica serovar Gallinarum biovar Pullorum and Gallinarum from chicken. Vet. World 2016, 9, 65–70. [Google Scholar] [CrossRef] [PubMed]
- Miles, T.D.; McLaughlin, W.; Brown, P.D. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet. Res. 2006, 2, 7. [Google Scholar] [CrossRef]
- Nguyen, V.T.; Carrique-Mas, J.J.; Ngo, T.H.; Ho, H.M.; Ha, T.T.; Campbell, J.I.; Nguyen, T.N.; Hoang, N.N.; Pham, V.M.; Wagenaar, J.A.; et al. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. J. Antimicrob. Chemother. 2015, 70, 2144–2152. [Google Scholar] [CrossRef]
- Ibrahim, S.; Wei Hoong, L.; Lai Siong, Y.; Mustapha, Z.; Zalati, C.W.S.; Aklilu, E.; Mohamad, M.; Kamaruzzaman, N.F. Prevalence of Antimicrobial Resistance (AMR) Salmonella spp. and Escherichia coli Isolated from Broilers in the East Coast of Peninsular Malaysia. Antibiotics 2021, 10, 579. [Google Scholar] [CrossRef]
- Baker, S.; Bryant, J.E.; Campbell, J.; Carrique-Mas, J.J.; Cuong, N.V.; Duy, D.T.; Hien, V.B.; Hoa, N.T.; Hoang, N.V.M.; Kiet, B.T.; et al. High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam. Epidemiol. Infect. 2015, 143, 3074–3086. [Google Scholar] [CrossRef]
- Hasan, B.; Swedberg, G. Molecular Characterization of Clinically Relevant Extended-Spectrum β-Lactamases bla(CTX-M-15)-Producing Enterobacteriaceae Isolated from Free-Range Chicken from Households in Bangladesh. Microb. Drug Resist. 2022, 28, 780–786. [Google Scholar] [CrossRef]
- Marr, I.; Sarmento, N.; O’Brien, M.; Lee, K.; Gusmao, C.; de Castro, G.; Janson, S.; Tong, S.Y.C.; Baird, R.W.; Francis, J.R. Antimicrobial resistance in urine and skin isolates in Timor-Leste. J. Glob. Antimicrob. Resist. 2018, 13, 135–138. [Google Scholar] [CrossRef]
- Oakley, T.; Le, B.; da Conceicao, V.; Marr, I.; Maia, C.; Soares, M.; Belo, J.C.; Sarmento, N.; da Silva, E.; Amaral, S.; et al. Gastrointestinal Carriage of Antimicrobial Resistance in School-Aged Children in Three Municipalities of Timor-Leste. Antibiotics 2022, 11, 1262. [Google Scholar] [CrossRef]
- Hedman, H.D.; Vasco, K.A.; Zhang, L. A Review of Antimicrobial Resistance in Poultry Farming within Low-Resource Settings. Animals 2020, 10, 1264. [Google Scholar] [CrossRef]
- Kim, Y.; Biswas, P.K.; Giasuddin, M.; Hasan, M.; Mahmud, R.; Chang, Y.M.; Essen, S.; Samad, M.A.; Lewis, N.S.; Brown, I.H.; et al. Prevalence of Avian Influenza A(H5) and A(H9) Viruses in Live Bird Markets, Bangladesh. Emerg. Infect. Dis. 2018, 24, 2309–2316. [Google Scholar] [CrossRef]
- Harris, P.A.; Taylor, R.; Minor, B.L.; Elliott, V.; Fernandez, M.; O’Neal, L.; McLeod, L.; Delacqua, G.; Delacqua, F.; Kirby, J.; et al. The REDCap consortium: Building an international community of software platform partners. J. Biomed. Inform. 2019, 95, 103208. [Google Scholar] [CrossRef]
- Harris, P.A.; Taylor, R.; Thielke, R.; Payne, J.; Gonzalez, N.; Conde, J.G. Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J. Biomed. Inform. 2009, 42, 377–381. [Google Scholar] [CrossRef]
- CLSI. Perfromance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, 4th ed.; CLSI Standard VET08; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2018. [Google Scholar]
- Sarmento, N.; Oakley, T.; Da Silva, E.S.; Tilman, A.; Monteiro, M.; Alves, L.; Barreto, I.; Marr, I.; Draper, A.D.; de Castro Hall, G. Strong relationships between the Northern Territory of Australia and Timor-Leste. Microbiol. Aust. 2022, 43, 125–129. [Google Scholar] [CrossRef]
- European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 13.0. 2023. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_13.0_Breakpoint_Tables.pdf (accessed on 20 November 2023).
- CLSI. Performance Standards for Antimicrobial Susceptibility Testing, 33rd ed.; CLSI Standard M100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2023. [Google Scholar]
- Schwarz, S.; Silley, P.; Simjee, S.; Woodford, N.; van Duijkeren, E.; Johnson, A.P.; Gaastra, W. Editorial: Assessing the antimicrobial susceptibility of bacteria obtained from animals. J. Antimicrob. Chemother. 2010, 65, 601–604. [Google Scholar] [CrossRef]
- European Committee on Antimicrobial Susceptibility Testing. EUCAST Guidelines for Detection of Resistance Mechanisms and Specific Resistances of Clinical and/or Epidemiological Importance. Version 2.0. 2017. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Resistance_mechanisms/EUCAST_detection_of_resistance_mechanisms_170711.pdf (accessed on 21 November 2023).
- StataCorp. Stata Statistical Software: Release 17; StataCorp LLC.: College Station, TX, USA, 2021. [Google Scholar]
- Ministry of Health. Timor-Leste Antimicrobial Guidelines. 2022. Available online: https://apps.ms.gov.tl/moh5/anti_e/handbook_eng.pdf (accessed on 10 September 2023).
- Kaper, J.B.; Nataro, J.P.; Mobley, H.L.T. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2, 123–140. [Google Scholar] [CrossRef]
- Liu, C.; Wang, P.; Dai, Y.; Liu, Y.; Song, Y.; Yu, L.; Feng, C.; Liu, M.; Xie, Z.; Shang, Y.; et al. Longitudinal monitoring of multidrug resistance in Escherichia coli on broiler chicken fattening farms in Shandong, China. Poult. Sci. 2021, 100, 100887. [Google Scholar] [CrossRef]
- Eltai, N.O.; Abdfarag, E.A.; Al-Romaihi, H.; Wehedy, E.; Mahmoud, M.H.; Alawad, O.K.; Al-Hajri, M.M.; Al Thani, A.A.; Yassine, H.M. Antibiotic Resistance Profile of Commensal Escherichia coli Isolated from Broiler Chickens in Qatar. J. Food Prot. 2018, 81, 302–307. [Google Scholar] [CrossRef]
- Jajere, S.M.; Hassan, L.; Abdul Aziz, S.; Zakaria, Z.; Abu, J.; Nordin, F.; Faiz, N.M. Salmonella in native “village” chickens (Gallus domesticus): Prevalence and risk factors from farms in South-Central Peninsular Malaysia. Poult. Sci. 2019, 98, 5961–5970. [Google Scholar] [CrossRef]
- Leotta, G.A.; Suzuki, K.; Alvarez, F.; Nuñez, L.; Silva, M.; Castro, L.; Faccioli, M.; Zarate, N.; Weiler, N.; Alvarez, M. Prevalence of Salmonella spp. in backyard chickens in Paraguay. Int. J. Poult. Sci. 2010, 9, 533–536. [Google Scholar] [CrossRef]
- Jafari, R.; Ghorbanpour, M.; Jaideri, A. An investigation into Salmonella infection status in backyard chickens in Iran. Int. J. Poult. Sci. 2007, 6, 227–229. [Google Scholar] [CrossRef]
- Soria, M.C.; Soria, M.A.; Bueno, D.J.; Godano, E.I.; Gómez, S.C.; ViaButron, I.A.; Padin, V.M.; Rogé, A.D. Salmonella spp. contamination in commercial layer hen farms using different types of samples and detection methods. Poult. Sci. 2017, 96, 2820–2830. [Google Scholar] [CrossRef]
- Sodagari, H.R.; Habib, I.; Whiddon, S.; Wang, P.; Mohammed, A.B.; Robertson, I.; Goodchild, S. Occurrence and Characterization of Salmonella Isolated from Table Egg Layer Farming Environments in Western Australia and Insights into Biosecurity and Egg Handling Practices. Pathogens 2020, 9, 56. [Google Scholar] [CrossRef]
- Samper-Cativiela, C.; Prieto, M.E.; Collado, S.; De Frutos, C.; Branscum, A.J.; Saez, J.L.; Alvarez, J. Risk Factors for Salmonella Detection in Commercial Layer Flocks in Spain. Animals 2023, 13, 3181. [Google Scholar] [CrossRef]
- Foley, S.L.; Nayak, R.; Hanning, I.B.; Johnson, T.J.; Han, J.; Ricke, S.C. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Appl. Environ. Microbiol. 2011, 77, 4273–4279. [Google Scholar] [CrossRef]
- Pacholewicz, E.; Wisselink, H.J.; Koene, M.G.J.; van der Most, M.; Gonzales, J.L. Environmental Sampling Methods for Detection of Salmonella Infections in Laying Hens: A Systematic Review and Meta-Analysis. Microorganisms 2023, 11, 2100. [Google Scholar] [CrossRef]
- Mueller-Doblies, D.; Sayers, A.R.; Carrique-Mas, J.J.; Davies, R.H. Comparison of sampling methods to detect Salmonella infection of turkey flocks. J. Appl. Microbiol. 2009, 107, 635–645. [Google Scholar] [CrossRef]
- Carrique-Mas, J.J.; Davies, R.H. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: A review. Rev. Sci. Tech. 2008, 27, 665–677. [Google Scholar] [CrossRef]
- Hedman, H.D.; Eisenberg, J.N.S.; Trueba, G.; Rivera, D.L.V.; Herrera, R.A.Z.; Barrazueta, J.V.; Rodriguez, G.I.G.; Krawczyk, E.; Berrocal, V.J.; Zhang, L. Impacts of small-scale chicken farming activity on antimicrobial-resistant Escherichia coli carriage in backyard chickens and children in rural Ecuador. One Health 2019, 8, 100112. [Google Scholar] [CrossRef]
- Kamboh, A.A.; Shoaib, M.; Abro, S.H.; Khan, M.A.; Malhi, K.K.; Yu, S. Antimicrobial Resistance in Enterobacteriaceae Isolated from Liver of Commercial Broilers and Backyard Chickens. J. Appl. Poult. Res. 2018, 27, 627–634. [Google Scholar] [CrossRef]
- Saeed, M.A.; Saqlain, M.; Waheed, U.; Ehtisham-ul-Haque, S.; Khan, A.U.; Rehman, A.u.; Sajid, M.; Atif, F.A.; Neubauer, H.; El-Adawy, H. Cross-Sectional Study for Detection and Risk Factor Analysis of ESBL-Producing Avian Pathogenic Escherichia coli Associated with Backyard Chickens in Pakistan. Antibiotics 2023, 12, 934. [Google Scholar] [CrossRef]
- Millar, J.; Morais, O.; Da Silva, H.; Hick, P.; Foster, A.; Jong, J.B.d.C.; Pereira, A.; Ting, S.; da Conceição, F.; Toribio, J.-A.L.M.L. Community engagement strengthens pig disease knowledge and passive surveillance in Timor-Leste. Front. Vet. Sci. 2023, 9, 1024094. [Google Scholar] [CrossRef]
- Usui, M.; Ozawa, S.; Onozato, H.; Kuge, R.; Obata, Y.; Uemae, T.; Ngoc, P.T.; Heriyanto, A.; Chalemchaikit, T.; Makita, K.; et al. Antimicrobial susceptibility of indicator bacteria isolated from chickens in Southeast Asian countries (Vietnam, Indonesia and Thailand). J. Vet. Med. Sci. 2014, 76, 685–692. [Google Scholar] [CrossRef]
- Coyne, L.; Patrick, I.; Arief, R.; Benigno, C.; Kalpravidh, W.; McGrane, J.; Schoonman, L.; Sukarno, A.H.; Rushton, J. The Costs, Benefits and Human Behaviours for Antimicrobial Use in Small Commercial Broiler Chicken Systems in Indonesia. Antibiotics 2020, 9, 154. [Google Scholar] [CrossRef]
- Zalizar, L.; Relawati, R.; Pancapalaga, W. Usage of Antibiotic on Chicken Poultry in District of Malang, East Java, Indonesia. In Proceedings of the International Seminar “Improving Tropical Production for Food Security”, Kendari, Indonesia, 3–5 November 2015; p. 158. [Google Scholar]
- Hardiati, A.; Safika, S.; Wibawan, I.W.T.; Indrawati, A.; Pasaribu, F.H. Isolation and detection of antibiotics resistance genes of Escherichia coli from broiler farms in Sukabumi, Indonesia. J. Adv. Vet. Anim. Res. 2021, 8, 84–90. [Google Scholar] [CrossRef]
- Moreno, M.A.; García-Soto, S.; Hernández, M.; Bárcena, C.; Rodríguez-Lázaro, D.; Ugarte-Ruíz, M.; Domínguez, L. Day-old chicks are a source of antimicrobial resistant bacteria for laying hen farms. Vet. Microbiol. 2019, 230, 221–227. [Google Scholar] [CrossRef]
- Coppola, N.; Cordeiro, N.F.; Trenchi, G.; Esposito, F.; Fuga, B.; Fuentes-Castillo, D.; Lincopan, N.; Iriarte, A.; Bado, I.; Vignoli, R. Imported One-Day-Old Chicks as Trojan Horses for Multidrug-Resistant Priority Pathogens Harboring mcr-9, rmtG, and Extended-Spectrum β-Lactamase Genes. Appl. Environ. Microbiol. 2022, 88, e0167521. [Google Scholar] [CrossRef]
- Okorafor, O.N.; Anyanwu, M.U.; Nwafor, E.O.; Anosa, G.N.; Udegbunam, R.I. Multidrug-resistant enterobacteria colonize commercial day-old broiler chicks in Nigeria. Vet. World 2019, 12, 418–423. [Google Scholar] [CrossRef]
- Dougnon, P.; Dougnon, V.; Legba, B.; Fabiyi, K.; Soha, A.; Koudokpon, H.; Sintondji, K.; Deguenon, E.; Hounmanou, G.; Quenum, C.; et al. Antibiotic profiling of multidrug resistant pathogens in one-day-old chicks imported from Belgium to benin. BMC Vet. Res. 2023, 19, 17. [Google Scholar] [CrossRef]
- Elmi, S.A.; Simons, D.; Elton, L.; Haider, N.; Abdel Hamid, M.M.; Shuaib, Y.A.; Khan, M.A.; Othman, I.; Kock, R.; Osman, A.Y. Identification of Risk Factors Associated with Resistant Escherichia coli Isolates from Poultry Farms in the East Coast of Peninsular Malaysia: A Cross Sectional Study. Antibiotics 2021, 10, 117. [Google Scholar] [CrossRef]
- Matuschek, E.; Åhman, J.; Webster, C.; Kahlmeter, G. Antimicrobial susceptibility testing of colistin—Evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin. Microbiol. Infect. 2018, 24, 865–870. [Google Scholar] [CrossRef]
- European Committee on Antimicrobial Susceptibility Testing. Antimicrobial Susceptibility Testing of Colistin—Problems Detected with Several Commercially Available Products. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Warnings/Warnings_docs/Warning_-_colistin_AST.pdf (accessed on 20 October 2023).
- Anantharajah, A.; Glupczynski, Y.; Hoebeke, M.; Bogaerts, P.; Declercq, P.; Denis, O.; Descy, J.; Floré, K.; Magerman, K.; Rodriguez-Villalobos, H.; et al. Multicenter study of automated systems for colistin susceptibility testing. Eur. J. Clin. Microbiol. Infect. Dis. 2021, 40, 575–579. [Google Scholar] [CrossRef]
- Bhatia, M.; Shamanna, V.; Nagaraj, G.; Gupta, P.; Omar, B.J.; Diksha; Chaudhary, R.; Ravikumar, K.L. Assessment of in vitro colistin susceptibility of Carbapenem-resistant clinical Gram-negative bacterial isolates using four commercially available systems & Whole-genome sequencing: A diagnostic accuracy study. Diagn. Microbiol. Infect. Dis. 2023, 108, 116155. [Google Scholar] [CrossRef]
- Zhang, Q.; Yan, W.; Zhu, Y.; Jing, N.; Wang, S.; Yuan, Y.; Ma, B.; Xu, J.; Chu, Y.; Zhang, J.; et al. Evaluation of Commercial Products for Colistin and Polymyxin B Susceptibility Testing for mcr-Positive and Negative Escherichia coli and Klebsiella pneumoniae in China. Infect. Drug Resist. 2023, 16, 1171–1181. [Google Scholar] [CrossRef]
- Brătfelan, D.O.; Tabaran, A.; Colobatiu, L.; Mihaiu, R.; Mihaiu, M. Prevalence and Antimicrobial Resistance of Escherichia coli Isolates from Chicken Meat in Romania. Animals 2023, 13, 3488. [Google Scholar] [CrossRef]
- Kempf, I.; Fleury, M.A.; Drider, D.; Bruneau, M.; Sanders, P.; Chauvin, C.; Madec, J.-Y.; Jouy, E. What do we know about resistance to colistin in Enterobacteriaceae in avian and pig production in Europe? Int. J. Antimicrob. Agents 2013, 42, 379–383. [Google Scholar] [CrossRef]
- Kempf, I.; Jouy, E.; Chauvin, C. Colistin use and colistin resistance in bacteria from animals. Int. J. Antimicrob. Agents 2016, 48, 598–606. [Google Scholar] [CrossRef]
- Dawadi, P.; Bista, S.; Bista, S. Prevalence of Colistin-Resistant Escherichia coli from Poultry in South Asian Developing Countries. Vet. Med. Int. 2021, 2021, 6398838. [Google Scholar] [CrossRef]
- Apostolakos, I.; Piccirillo, A. A review on the current situation and challenges of colistin resistance in poultry production. Avian Pathol. 2018, 47, 546–558. [Google Scholar] [CrossRef]
- World Health Organization. Critically Important Antimicrobials for Human Medicine: 6th Revision; World Health Organization: Geneva, Switzerland, 2019. [Google Scholar]
- World Organisation for Animal Health. OIE List of Antimicrobial Agents of Veterinary Importance (June 2021). Available online: https://www.woah.org/app/uploads/2021/06/a-oie-list-antimicrobials-june2021.pdf (accessed on 19 October 2023).
- Al-Tawfiq, J.A.; Laxminarayan, R.; Mendelson, M. How should we respond to the emergence of plasmid-mediated colistin resistance in humans and animals? Int. J. Infect. Dis. 2017, 54, 77–84. [Google Scholar] [CrossRef]
- Harris, L.; Bongers, A.; Yan, J.; Francis, J.R.; Marr, I.; Lake, S.; Martins, S. Estimates of Antibacterial Consumption in Timor-Leste Using Distribution Data and Variation in Municipality Usage Patterns. Antibiotics 2021, 10, 1468. [Google Scholar] [CrossRef]
- Chen, Z.; Bai, J.; Zhang, X.; Wang, S.; Chen, K.; Lin, Q.; Xu, C.; Qu, X.; Zhang, H.; Liao, M.; et al. Highly prevalent multidrug resistance and QRDR mutations in Salmonella isolated from chicken, pork and duck meat in Southern China, 2018–2019. Int. J. Food Microbiol. 2021, 340, 109055. [Google Scholar] [CrossRef]
- Lu, Y.; Wu, C.M.; Wu, G.J.; Zhao, H.Y.; He, T.; Cao, X.Y.; Dai, L.; Xia, L.N.; Qin, S.S.; Shen, J.Z. Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China. Foodborne Pathog. Dis. 2011, 8, 45–53. [Google Scholar] [CrossRef]
- Chaudhary, P.; Salam, S.m.A.; Reza, M.A.; Ahaduzzaman, M. High prevalence of ciprofloxacin and ceftriaxone resistance Salmonella in the retail chicken market of Chattogram, Bangladesh. Turk. J. Vet. Res. 2019, 3, 51–55. [Google Scholar]
- Sharma, J.; Kumar, D.; Hussain, S.; Pathak, A.; Shukla, M.; Prasanna Kumar, V.; Anisha, P.N.; Rautela, R.; Upadhyay, A.K.; Singh, S.P. Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control 2019, 102, 104–111. [Google Scholar] [CrossRef]
- Rickert-Hartman, R.; Folster, J.P. Ciprofloxacin-resistant Salmonella enterica serotype Kentucky sequence type 198. Emerg. Infect. Dis. 2014, 20, 910–911. [Google Scholar] [CrossRef]
- Xiong, Z.; Wang, S.; Huang, Y.; Gao, Y.; Shen, H.; Chen, Z.; Bai, J.; Zhan, Z.; Wen, J.; Liao, M.; et al. Ciprofloxacin-Resistant Salmonella enterica Serovar Kentucky ST198 in Broiler Chicken Supply Chain and Patients, China, 2010–2016. Microorganisms 2020, 8, 140. [Google Scholar] [CrossRef]
- Vázquez, X.; Fernández, J.; Bances, M.; Lumbreras, P.; Alkorta, M.; Hernáez, S.; Prieto, E.; de la Iglesia, P.; de Toro, M.; Rodicio, M.R.; et al. Genomic Analysis of Ciprofloxacin-Resistant Salmonella enterica Serovar Kentucky ST198 From Spanish Hospitals. Front. Microbiol. 2021, 12, 720449. [Google Scholar] [CrossRef]
- Crump, J.A.; Sjölund-Karlsson, M.; Gordon, M.A.; Parry, C.M. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin. Microbiol. Rev. 2015, 28, 901–937. [Google Scholar] [CrossRef]
- Hopkins, K.L.; Davies, R.H.; Threlfall, E.J. Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. Int. J. Antimicrob. Agents 2005, 25, 358–373. [Google Scholar] [CrossRef]
- Bui, C.B.; Carrique-Mas, J.; Diep, T.Q.; Do, D.H.; Henry, W.; Hoang, N.V.; Inui, K.; Le, T.D.; Nguyen, T.T.; Phan, M.Q.; et al. Detection of HPAI H5N1 viruses in ducks sampled from live bird markets in Vietnam. Epidemiol. Infect. 2013, 141, 601–611. [Google Scholar] [CrossRef]
- Aenishaenslin, C.; Häsler, B.; Ravel, A.; Parmley, J.; Stärk, K.; Buckeridge, D. Evidence needed for antimicrobial resistance surveillance systems. Bull. World Health Organ. 2019, 97, 283–289. [Google Scholar] [CrossRef]
- Shittu, O.B.; Uzairue, L.I.; Ojo, O.E.; Obuotor, T.M.; Folorunso, J.B.; Raheem-Ademola, R.R.; Olanipekun, G.; Ajose, T.; Medugu, N.; Ebruke, B.; et al. Antimicrobial resistance and virulence genes in Salmonella enterica serovars isolated from droppings of layer chicken in two farms in Nigeria. J. Appl. Microbiol. 2022, 132, 3891–3906. [Google Scholar] [CrossRef] [PubMed]
- Kipper, D.; Mascitti, A.K.; De Carli, S.; Carneiro, A.M.; Streck, A.F.; Fonseca, A.S.K.; Ikuta, N.; Lunge, V.R. Emergence, Dissemination and Antimicrobial Resistance of the Main Poultry-Associated Salmonella Serovars in Brazil. Vet. Sci. 2022, 9, 405. [Google Scholar] [CrossRef] [PubMed]
- Ferrari, R.G.; Rosario, D.K.A.; Cunha-Neto, A.; Mano, S.B.; Figueiredo, E.E.S.; Conte-Junior, C.A. Worldwide Epidemiology of Salmonella Serovars in Animal-Based Foods: A Meta-analysis. Appl. Environ. Microbiol. 2019, 85, e00591-19. [Google Scholar] [CrossRef]
- Florio, W.; Baldeschi, L.; Rizzato, C.; Tavanti, A.; Ghelardi, E.; Lupetti, A. Detection of Antibiotic-Resistance by MALDI-TOF Mass Spectrometry: An Expanding Area. Front. Cell. Infect. Microbiol. 2020, 10, 572909. [Google Scholar] [CrossRef] [PubMed]
- Elabbasy, M.T.; Hussein, M.A.; Algahtani, F.D.; Abd El-Rahman, G.I.; Morshdy, A.E.; Elkafrawy, I.A.; Adeboye, A.A. MALDI-TOF MS Based Typing for Rapid Screening of Multiple Antibiotic Resistance E. coli and Virulent Non-O157 Shiga Toxin-Producing E. coli Isolated from the Slaughterhouse Settings and Beef Carcasses. Foods 2021, 10, 820. [Google Scholar] [CrossRef] [PubMed]
Location of Sampling | Origin of Sample | Number of Samples | E. coli | Salmonella spp. | ||
---|---|---|---|---|---|---|
Number of Isolates | Recovery Rate (%) | Number of Isolates | Recovery Rate (%) | |||
Live bird markets | Local chicken | 254 | 217 | 85.4 | 4 | 1.5 |
Fighting cock | 72 | 60 | 83.3 | 1 | 1.3 | |
Broiler | 17 | 16 | 94.1 | 3 | 17.6 | |
Layer | 2 | 2 | 100 | 0 | - | |
Total | 345 | 295 | 85.5 | 8 | 2.3 | |
Layer farms | Layer house | 87 | 74 | 85.1 | 29 | 33.3 |
Antimicrobial | E. coli Isolates | Salmonella spp. Isolates | ||
---|---|---|---|---|
Prevalence from LBMs (n = 295) (%) (95%CI) | Prevalence from LF (n = 74) (%) (95%CI) | Prevalence from LBMs (n = 8) (%) (95%CI) | Prevalence from LF (n = 29) (%) (95%CI) | |
Ampicillin | 16.6 (13.0–21.0) | 23.0 (13.7–35.8) | 25.0 (1.7–86.2) | 24.1 (8.5–52.2) |
Streptomycin | 7.8 (4.4–13.3) | 16.2 (8.9–27.8) | 25.0 (1.7–86.2) | 17.2 (3.4–55.0) |
Tetracycline | 16.3 (12.2–21.3) | 48.6 (38.4–60.0) | 75.0 (19.2–97.4) | 31.0 (12.3–59.2) |
Enrofloxacin | 0.7 (0.2–2.0) | 9.5 (4.2–20.0) | 25.0 (1.7–86.2) | 20.7 (9.5–39.3) |
Trimethoprim/Sulphamethoxazole | 8.8 (5.5–13.8) | 24.3 (15.6–35.9) | 25.0 (1.7–86.2) | 3.4 (0.8–14.0) |
Sulfisoxazole | 13.6 (8.1–21.7) | 29.7 (19.6–42.4) | 37.5 (5.5–86.2) | 20.7 (6.3–50.2) |
Multi-drug resistant | 7.8 (5.3–11.4) | 20.3 (9.7–37.5) | 25.0 (1.7–86.2) | 17.2 (3.4–55.0) |
Number of Antimicrobials | Phenotypic Resistance Profile | E. coli | Salmonella spp. | ||||
---|---|---|---|---|---|---|---|
Percent of Isolates from LBMs (n = 295) | Percent of Isolates from LFs (n = 74) | Percent of Isolates from LBMs and LFs (n = 369) | Percent of Isolates from LBMs (n = 8) | Percent of Isolates from LFs (n = 29) | Percent of Isolates from LBMs and LFs (n = 37) | ||
0 | None | 72.2 | 39.2 | 65.6 | 25.0 | 48.3 | 55.2 |
1 | AMP | 3.1 | 2.7 | 3.0 | 0 | 0 | 0 |
STR | 1.4 | 1.4 | 1.4 | 0 | 0 | 0 | |
TET | 2.0 | 14.9 | 4.6 | 37.5 | 13.8 | 24.1 | |
SXT | 0.3 | 0 | 0.3 | 0 | 0 | 0 | |
ENR | 0.3 | 1.4 | 0.5 | 0 | 10.3 | 10.3 | |
SOX | 2.4 | 0 | 1.9 | 0 | 3.4 | 3.4 | |
2 | AMP-TET | 5.1 | 2.7 | 4.6 | 0 | 0 | 0 |
AMP-SXT | 0.3 | 0 | 0.3 | 0 | 0 | 0 | |
AMP-ENR | 0 | 0 | 0 | 0 | 6.9 | 6.9 | |
STR-TET | 0 | 2.7 | 0.5 | 0 | 0 | 0 | |
STR-ENR | 0 | 1.4 | 0.3 | 0 | 0 | 0 | |
STR-SOX | 1.4 | 0 | 1.1 | 0 | 0 | 0 | |
TET-ENR | 0 | 2.7 | 0.5 | 0 | 0 | 0 | |
TET-SOX | 0.7 | 0 | 0.5 | 12.5 | 0 | 3.4 | |
SXT-SOX | 0.7 | 2.7 | 1.1 | 0 | 0 | 0 | |
3 | AMP-STR-TET | 0.3 | 1.4 | 0.5 | 0 | 0 | 0 |
AMP-STR-SOX | 0.3 | 0 | 0.3 | 0 | 0 | 0 | |
AMP-TET-SXT | 1.0 | 0 | 0.8 | 0 | 0 | 0 | |
AMP-TET-SOX | 0.7 | 4.1 | 1.4 | 0 | 0 | 0 | |
AMP-SXT-SOX | 0.7 | 0 | 0.5 | 0 | 0 | 0 | |
STR-TET-SOX | 0 | 1.4 | 0.3 | 0 | 0 | 0 | |
STR-SXT-SOX | 0 | 1.4 | 0.3 | 0 | 0 | 0 | |
TET-SXT-SOX | 1.7 | 6.8 | 2.7 | 0 | 0 | 0 | |
4 | AMP-STR-TET-SOX | 1.4 | 0 | 1.1 | 0 | 10.3 | 10.3 |
AMP-STR-SXT-SOX | 0.7 | 0 | 0.5 | 0 | 0 | 0 | |
AMP-TET-SXT-SOX | 1.0 | 4.1 | 1.6 | 0 | 0 | 0 | |
STR-TET-SXT-SOX | 0.3 | 1.4 | 0.5 | 0 | 0 | 0 | |
5 | AMP-STR-TET-SXT-ENR | 0.3 | 0 | 0.3 | 0 | 0 | 0 |
AMP-STR-TET-SXT-SOX | 1.7 | 4.1 | 2.2 | 0 | 3.4 | 3.4 | |
AMP-STR-TET-ENR-SOX | 0 | 0 | 0 | 0 | 3.4 | 3.4 | |
AMP-STR-SXT-ENR-SOX | 0 | 1.4 | 0.3 | 0 | 0 | 0 | |
AMP-TET-SXT-ENR-SOX | 0 | 2.7 | 0.5 | 0 | 0 | 0 | |
6 | AMP-STR-TET-SXT-ENR-SOX | 0 | 0 | 0 | 25.0 | 0 | 6.9 |
Antimicrobial Class/Antimicrobials | Percentage of Resistant Isolates (%) | MIC50 (mg/L) | MIC90 (mg/L) | ||
---|---|---|---|---|---|
LBMs and LFs (n = 212) | From LBMs Only (n = 169) | From LFs Only (n = 43) | |||
Penicillins | |||||
Ampicillin * | 22.2 | 18.9 | 34.9 | ≤2 | >8 |
Piperacillin | 17.0 | 14.2 | 27.9 | ≤4 | >64 |
Mecillinam | 8.5 | 10.1 | 2.3 | ≤2 | 8 |
Temocillin | 10.4 | 10.7 | 9.3 | 8 | 32 |
β-lactam/β-lactam inhibitor combination | |||||
Amoxicillin-Clavulanic acid * | 20.3 | 20.7 | 18.6 | 4 | 32 |
Piperacillin-Tazobactam * | 0.5 | 0.6 | 0 | ≤4 | ≤4 |
Cephalosporins | |||||
Cephalexin | 4.7 | 3.0 | 11.6 | 8 | 16 |
Cefepime | 5.2 | 5.9 | 2.3 | ≤1 | ≤1 |
Ceftriaxone * | 5.2 | 5.9 | 2.3 | ≤0.5 | ≤0.5 |
Cefuroxime * | 8.0 | 6.5 | 14.0 | 4 | 8 |
Ceftazidime | 3.8 | 4.1 | 2.3 | ≤0.5 | ≤0.5 |
Cefixime | 6.1 | 7.1 | 2.3 | ≤0.5 | 1 |
Monobactams | |||||
Aztreonam | 4.7 | 5.3 | 2.3 | ≤1 | ≤1 |
Carbapenems | |||||
Ertapenem | 0 | 0 | 0 | ≤0.25 | ≤0.25 |
Imipenem | 0.9 | 0.6 | 2.3 | 0.5 | 1 |
Meropenem * | 0 | 0 | 0 | ≤0.125 | 0.25 |
Polymyxin | |||||
Colistin | 6.6 | 6.5 | 7.0 | ≤0.5 | 1 |
Aminoglycosides | |||||
Gentamicin * | 5.7 | 5.9 | 4.7 | 2 | 2 |
Amikacin * | 0 | 0 | 0 | ≤4 | 8 |
Tobramycin | 4.7 | 4.7 | 4.7 | 2 | 2 |
Fluroquinolones | |||||
Ciprofloxacin * | 2.4 | 0.6 | 9.3 | ≤0.125 | ≤0.125 |
Levofloxacin * | 1.4 | 0.6 | 4.7 | ≤0.5 | ≤0.5 |
Sulfonamides | |||||
Trimethoprim-Sulfamethoxazole * | 8.0 | 4.7 | 20.9 | ≤1 | ≤1 |
Phosphonic acid | |||||
Fosfomycin w/G6P | 0.9 | 0 | 4.7 | ≤16 | ≤16 |
Nitrofuran | |||||
Nitrofurantoin * | 0.5 | 0 | 2.3 | ≤16 | 32 |
Multi-drug resistant | 13.7 | 11.8 | 20.9 | - | - |
Antimicrobial Class/Antimicrobials | Percentage of Resistant Isolates (%) | ||
---|---|---|---|
LBMs and LFs (n = 17) | From LBMs Only (n = 1) | From LFs Only (n = 16) | |
Penicillins | |||
Ampicillin * | 23.5 | 0 | 25.0 |
Piperacillin | 23.5 | 0 | 25.0 |
Mecillinam | 5.9 | 100 | 0 |
Temocillin | 41.2 | 0 | 43.8 |
β-lactam/β-lactam inhibitor combination | |||
Amoxicillin-Clavulanic acid * | 0 | 0 | 0 |
Piperacillin-Tazobactam * | 0 | 0 | 0 |
Cephalosporins | |||
Cephalexin | 0 | 0 | 0 |
Cefepime | 0 | 0 | 0 |
Ceftriaxone * | 0 | 0 | 0 |
Cefuroxime * | 5.9 | 0 | 6.3 |
Ceftazidime | 0 | 0 | 0 |
Cefixime | 0 | 0 | 0 |
Monobactams | |||
Aztreonam | 0 | 0 | 0 |
Carbapenems | |||
Ertapenem | 0 | 0 | 0 |
Imipenem | 5.9 | 100 | 0 |
Meropenem * | 0 | 0 | 0 |
Polymyxin | |||
Colistin | 5.9 | 100 | 0 |
Aminoglycosides | |||
Gentamicin * | 5.9 | 100 | 0 |
Amikacin * | 0 | 0 | 0 |
Tobramycin | 5.9 | 100 | 0 |
Fluroquinolones | |||
Ciprofloxacin * | 47.1 | 0 | 50.0 |
Levofloxacin * | 17.7 | 0 | 18.8 |
Sulfonamides | |||
Trimethoprim-Sulfamethoxazole * | 5.9 | 100 | 0 |
Phosphonic acid | |||
Fosfomycin w/G6P | 0 | 0 | 0 |
Nitrofuran | |||
Nitrofurantoin * | 0 | 0 | 0 |
Multi-drug resistant | 5.9 | 100 | 0 |
Antimicrobial/Origin of Isolate | Resistance (%) | Odds Ratio (95%CI) | p Value |
---|---|---|---|
Ampicillin | 0.017 | ||
Local chicken | 13.4 | Ref | |
Fighting cock | 21.7 | 1.8 (0.9–3.7) | 0.116 |
Broiler | 43.8 | 5.2 (1.7–16.0) | 0.004 |
Layer farm | 23.0 | 2.0 (1.0–4.0) | 0.066 |
Streptomycin | 0.008 | ||
Local chicken | 6.0 | Ref | |
Fighting cock | 8.3 | 1.5 (0.5–4.4) | 0.476 |
Broiler | 31.3 | 8.2 (2.2–30.1) | 0.002 |
Layer farm | 16.2 | 3.3 (1.1–9.7) | 0.028 |
Tetracycline | <0.001 | ||
Local chicken | 12.9 | Ref | |
Fighting cock | 18.3 | 1.5 (0.7–3.3) | 0.287 |
Broiler | 50.0 | 6.7 (2.3–19.4) | <0.001 |
Layer farm | 48.6 | 6.4 (3.5–11.7) | <0.001 |
Enrofloxacin | 0.003 | ||
Local chicken | 0.9 | Ref | |
Fighting cock | 0 | N/A | N/A |
Broiler | 0 | N/A | N/A |
Layer farm | 9.5 | 11.2 (2.3–55.4) | 0.003 |
Trimethoprim/sulfamethoxazole | <0.001 | ||
Local chicken | 6.5 | Ref | |
Fighting cock | 8.3 | 1.3 (0.5–3.8) | 0.611 |
Broiler | 62.5 | 8.7 (2.8–27.4) | <0.001 |
Layer farm | 29.7 | 4.7 (2.2–10.0) | <0.001 |
Sulfixosazole | <0.001 | ||
Local chicken | 8.8 | Ref | |
Fighting cock | 16.7 | 2.1 (0.9–4.8) | 0.081 |
Broiler | 62.5 | 17.4 (5.7–53.0) | <0.001 |
Layer farm | 29.7 | 4.4 (2.2–8.8) | <0.001 |
Multi-drug resistant | <0.001 | ||
Local chicken | 4.6 | Ref | |
Fighting cock | 10.0 | 2.3 (0.8–6.5) | 0.131 |
Broiler | 43.8 | 18.1 (5.3–61.2) | <0.001 |
Layer farm | 20.3 | 5.2 (2.0–13.1) | 0.001 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pereira, A.; Sidjabat, H.E.; Davis, S.; Vong da Silva, P.G.; Alves, A.; Dos Santos, C.; Jong, J.B.d.C.; da Conceição, F.; Felipe, N.d.J.; Ximenes, A.; et al. Prevalence of Antimicrobial Resistance in Escherichia coli and Salmonella Species Isolates from Chickens in Live Bird Markets and Boot Swabs from Layer Farms in Timor-Leste. Antibiotics 2024, 13, 120. https://doi.org/10.3390/antibiotics13020120
Pereira A, Sidjabat HE, Davis S, Vong da Silva PG, Alves A, Dos Santos C, Jong JBdC, da Conceição F, Felipe NdJ, Ximenes A, et al. Prevalence of Antimicrobial Resistance in Escherichia coli and Salmonella Species Isolates from Chickens in Live Bird Markets and Boot Swabs from Layer Farms in Timor-Leste. Antibiotics. 2024; 13(2):120. https://doi.org/10.3390/antibiotics13020120
Chicago/Turabian StylePereira, Abrao, Hanna E. Sidjabat, Steven Davis, Paulo Gabriel Vong da Silva, Amalia Alves, Cristibela Dos Santos, Joanita Bendita da Costa Jong, Felisiano da Conceição, Natalino de Jesus Felipe, Augusta Ximenes, and et al. 2024. "Prevalence of Antimicrobial Resistance in Escherichia coli and Salmonella Species Isolates from Chickens in Live Bird Markets and Boot Swabs from Layer Farms in Timor-Leste" Antibiotics 13, no. 2: 120. https://doi.org/10.3390/antibiotics13020120
APA StylePereira, A., Sidjabat, H. E., Davis, S., Vong da Silva, P. G., Alves, A., Dos Santos, C., Jong, J. B. d. C., da Conceição, F., Felipe, N. d. J., Ximenes, A., Nunes, J., Fária, I. d. R., Lopes, I., Barnes, T. S., McKenzie, J., Oakley, T., Francis, J. R., Yan, J., & Ting, S. (2024). Prevalence of Antimicrobial Resistance in Escherichia coli and Salmonella Species Isolates from Chickens in Live Bird Markets and Boot Swabs from Layer Farms in Timor-Leste. Antibiotics, 13(2), 120. https://doi.org/10.3390/antibiotics13020120