Poultry as Hidden Reservoirs: The Growing Public Health Threat of Resistant Enterobacteriaceae
Main Article Content
Abstract
The widespread use of antimicrobials in poultry production for therapeutic and non-therapeutic purposes has resulted in the emergence and dissemination of multidrug-resistant (MDR) Enterobacteriaceae, such as Escherichia coli, Klebsiella spp., Proteus spp., and Salmonella spp. These organisms, routinely found in poultry and their environments, carry a variety of resistance genes that can be transferred to humans through the food chain, environmental contamination, and direct contact. The consequences of these resistance genes are profound, leading to increased morbidity and mortality associated with resistant infections. As a result, the effectiveness of last-resort antibiotics is compromised, resulting in the need for more expensive and less effective treatments, posing a substantial economic burden on healthcare systems. In this review, we discuss the resistance genes present in poultry and its environment, modes of transmission and acquisition of these resistance genes, and associated public health implications. It emphasizes the need for enhanced surveillance, alternative management strategies in poultry farming, and coordinated global efforts to mitigate the public health threat posed by resistant Enterobacteriaceae.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Muteeb G, Rehman MT, Shahwan M, Aatif M. Origin of Antibiotics and Antibiotic Resistance, and Their Impacts on Drug Development: A Narrative Review. Pharmaceuticals. 2023;16(11):1–54.
WHO. Global action plan on antimicrobial resistance. World Heal Organ. 2017;1–28.
Uddin TM, Chakraborty AJ, Khusro A, Zidan BMRM, Mitra S, Emran T Bin, et al. Antibiotic resistance in microbes: History, mechanisms, therapeutic strategies and future prospects. J Infect Public Health [Internet]. 2021;14(12):1750–66. Available from: https://www.sciencedirect.com/science/article/pii/S1876034121003403
Ahmed SK, Hussein S, Qurbani K, Ibrahim RH, Fareeq A, Mahmood KA, et al. Antimicrobial resistance: Impacts, challenges, and future prospects. J Med Surgery, Public Heal [Internet]. 2024;2(January):100081. Available from: https://doi.org/10.1016/j.glmedi.2024.100081
Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55.
Fam N, Opin C, Comm J, Iii JJF, Control D, Diseases D, et al. Enterobacteriaceae. 2015;
K. RA, M. MA. Enterobacterial Common Antigen: Synthesis and Function of an Enigmatic Molecule. MBio [Internet]. 2020 Aug 11;11(4):10.1128/mbio.01914-20. Available from: https://doi.org/10.1128/mbio.01914-20
Borman EK, Stuart CA, Wheeler KM. TAXONOMY OF THE FAMILY ENTEROBACTERIACEAE. 1944;
Palusiak A. Proteus mirabilis and Klebsiella pneumoniae as pathogens capable of causing co-infections and exhibiting similarities in their virulence factors. Front Cell Infect Microbiol. 2022;12:991657.
Coipan CE, Westrell T, van Hoek AHAM, Alm E, Kotila S, Berbers B, et al. Genomic epidemiology of emerging ESBL-producing Salmonella Kentucky bla CTX-M-14b in Europe. Emerg Microbes Infect [Internet]. 2020;9(1):2124–35. Available from: https://doi.org/10.1080/22221751.2020.1821582
Partridge SR. Resistance mechanisms in Enterobacteriaceae. Pathology. 2015;47(3):276–84.
Leinyuy JF, Ali IM, Karimo O, Tume CB. Patterns of Antibiotic Resistance in Enterobacteriaceae Isolates from Broiler Chicken in the West Region of Cameroon : A Cross-Sectional Study. 2022;2022.
Wright GD. Mechanisms of resistance to antibiotics. Curr Opin Chem Biol. 2003;7(5):563–9.
Denton M. Enterobacteriaceae. Int J Antimicrob Agents. 2007;29(SUPPL. 3).
Wang Y, Lyu N, Liu F, Liu WJ, Bi Y, Zhang Z, et al. More diversified antibiotic resistance genes in chickens and workers of the live poultry markets. Environ Int [Internet]. 2021;153:106534. Available from: https://www.sciencedirect.com/science/article/pii/S0160412021001598
Urban-Chmiel R, Marek A, Stępień-Pyśniak D, Wieczorek K, Dec M, Nowaczek A, et al. Antibiotic Resistance in Bacteria-A Review. Antibiot (Basel, Switzerland). 2022 Aug;11(8).
Jean SS, Harnod D, Hsueh PR. Global Threat of Carbapenem-Resistant Gram-Negative Bacteria. Front Cell Infect Microbiol. 2022;12(March):1–19.
Vardakas KZ, Tansarli GS, Rafailidis PI, Falagas ME. Carbapenems versus alternative antibiotics for the treatment of bacteraemia due to enterobacteriaceae producing extended-spectrum β-lactamases: A systematic review and meta-analysis. J Antimicrob Chemother. 2012;67(12):2793–803.
Sharma E, Chen Y, Kelso C, Sivakumar M, Jiang G. Colistin and carbapenems as last-resort antibiotics: Challenging environmental impacts and analytical methods. Soil Environ Heal [Internet]. 2024;2(1):100058. Available from: https://doi.org/10.1016/j.seh.2024.100058
Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH. Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: A global perspective. Clin Microbiol Infect. 2012;18(7):646–55.
van Hoek AHAM, Veenman C, van Overbeek WM, Lynch G, de Roda Husman AM, Blaak H. Prevalence and characterization of ESBL- and AmpC-producing Enterobacteriaceae on retail vegetables. Int J Food Microbiol [Internet]. 2015;204:1–8. Available from: http://dx.doi.org/10.1016/j.ijfoodmicro.2015.03.014
Reist M, Geser N, Hächler H, Schärrer S, Stephan R. ESBL-Producing Enterobacteriaceae: Occurrence, Risk Factors for Fecal Carriage and Strain Traits in the Swiss Slaughter Cattle Population Younger than 2 Years Sampled at Abattoir Level. PLoS One. 2013;8(8).
Eibach D, Dekker D, Gyau Boahen K, Wiafe Akenten C, Sarpong N, Belmar Campos C, et al. Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in local and imported poultry meat in Ghana. Vet Microbiol [Internet]. 2018;217(January):7–12. Available from: https://doi.org/10.1016/j.vetmic.2018.02.023
Dossouvi KM, Ametepe AS. Carbapenem Resistance in Animal-Environment-Food from Africa: A Systematic Review, Recommendations and Perspectives. Infect Drug Resist. 2024;17:1699–728.
Wareth G, Neubauer H. The Animal-foods-environment interface of Klebsiella pneumoniae in Germany: an observational study on pathogenicity, resistance development and the current situation. Vet Res [Internet]. 2021;52(1):1–14. Available from: https://doi.org/10.1186/s13567-020-00875-w
Girlich D, Bonnin RA, Dortet L, Naas T. Genetics of Acquired Antibiotic Resistance Genes in Proteus spp. Front Microbiol. 2020;11(February):1–21.
Hubbard LE, Givens CE, Griffin DW, Iwanowicz LR, Meyer MT, Kolpin DW. Poultry litter as potential source of pathogens and other contaminants in groundwater and surface water proximal to large-scale confined poultry feeding operations. Sci Total Environ [Internet]. 2020;735:139459. Available from: https://doi.org/10.1016/j.scitotenv.2020.139459
Abbassi MS, Kilani H, Abid I, Sáenz Y, Hynds P, Lengliz S, et al. Genetic Background of Antimicrobial Resistance in Multiantimicrobial-Resistant Escherichia coli Isolates from Feces of Healthy Broiler Chickens in Tunisia. Biomed Res Int. 2021;2021.
Machado E, Coque TM, Cantón R, Sousa JC, Peixe L. Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J Antimicrob Chemother. 2008;62(2):296–302.
Djeffal S, Bakour S, Mamache B, Elgroud R, Agabou A, Chabou S, et al. Prevalence and clonal relationship of ESBL-producing Salmonella strains from humans and poultry in northeastern Algeria. BMC Vet Res. 2017;13(1):1–9.
Nordmann P. Carbapenemase-producing Enterobacteriaceae: Overview of a major public health challenge. Med Mal Infect [Internet]. 2014;44(2):51–6. Available from: http://dx.doi.org/10.1016/j.medmal.2013.11.007
Racewicz P, Majewski M, Biesiada H, Nowaczewski S, Wilczyński J, Wystalska D, et al. Prevalence and characterisation of antimicrobial resistance genes and class 1 and 2 integrons in multiresistant Escherichia coli isolated from poultry production. Sci Rep [Internet]. 2022;12(1):1–13. Available from: https://doi.org/10.1038/s41598-022-09996-y
Li Z, Peng C, Zhang G, Shen Y, Zhang Y, Liu C, et al. Prevalence and characteristics of multidrug-resistant Proteus mirabilis from broiler farms in Shandong Province, China. Poult Sci. 2022;101710.
Savin M, Bierbaum G, Blau K, Parcina M, Sib E, Smalla K, et al. Colistin-Resistant Enterobacteriaceae Isolated From Process Waters and Wastewater From German Poultry and Pig Slaughterhouses. Front Microbiol. 2020;11(October).
Ayinla AO, Mateus ALP. Extended-spectrum beta-lactamases in poultry in Africa: a systematic review. Front Antibiot. 2023;2(May).
Amábile-Cuevas CF, Lund-Zaina S. Non-Canonical Aspects of Antibiotics and Antibiotic Resistance. Antibiot (Basel, Switzerland). 2024 Jun;13(6).
de Oliveira D V., Van Der Sand ST. Phenotypic Tests for the Detection of β-Lactamase-Producing Enterobacteriaceae Isolated from Different Environments. Curr Microbiol. 2016;73(1):132–8.
Tao S, Chen H, Li N, Wang T, Liang W. The Spread of Antibiotic Resistance Genes In Vivo Model. Can J Infect Dis Med Microbiol. 2022;2022.
Von Wintersdorff CJH, Penders J, Van Niekerk JM, Mills ND, Majumder S, Van Alphen LB, et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front Microbiol. 2016;7(FEB):1–10.
Virolle C, Goldlust K, Djermoun S, Bigot S, Lesterlin C. Plasmid transfer by conjugation in gram-negative bacteria: From the cellular to the community level. Genes (Basel). 2020;11(11):1–33.
Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, de la Cruz F. Mobility of Plasmids. Microbiol Mol Biol Rev. 2010;74(3):434–52.
Nadeem SF, Gohar UF, Tahir SF, Mukhtar H, Pornpukdeewattana S, Nukthamna P, et al. Antimicrobial resistance: more than 70 years of war between humans and bacteria. Crit Rev Microbiol [Internet]. 2020;46(5):578–99. Available from: https://doi.org/10.1080/1040841X.2020.1813687
Saliu EM, Zentek J, Vahjen W. In vitro conjugation kinetics of AmpC, broad spectrum and extended-spectrum beta-lactamase-producing Escherichia coli donors and various Enterobacteriaceae recipients. BMC Microbiol. 2020;20(1):4–11.
Adeleye IA. Conjugal Transferability of Multiple Antibiotic Resistance in Three Genera of Enterobacteriaceae in Nigeria. J Diarrhoeal Dis Res [Internet]. 1992 Feb 27;10(2):93–6. Available from: http://www.jstor.org/stable/23498149
Liu X, Yang X, Ye L, Chan EWC, Chen S. Genetic Characterization of a Conjugative Plasmid That Encodes Azithromycin Resistance in Enterobacteriaceae. Microbiol Spectr. 2022 Jun;10(3):e0078822.
Sølverød MS, Marianne S, Karin IH, Solveig L, Even H. Transfer Potential of Plasmids Conferring Extended-Spectrum-Cephalosporin Resistance in Escherichia coli from Poultry. Appl Environ Microbiol [Internet]. 2017 May 31;83(12):e00654-17. Available from: https://doi.org/10.1128/AEM.00654-17
Overballe-Petersen S, Harms K, Orlando LAA, Moreno Mayar J V., Rasmussen S, Dahl TW, et al. Bacterial natural transformation by highly fragmented and damaged DNA. Proc Natl Acad Sci U S A. 2013;110(49):19860–5.
Touzain F, Le Devendec L, de Boisséson C, Baron S, Jouy E, Perrin-Guyomard A, et al. Characterization of plasmids harboring blaCTX-M and blaCMY genes in E. coli from French broilers. PLoS One [Internet]. 2018 Jan 23;13(1):e0188768. Available from: https://doi.org/10.1371/journal.pone.0188768
Vaidya VK. Horizontal Transfer of Antimicrobial Resistance by Extended-Spectrum β Lactamase-Producing Enterobacteriaceae. J Lab Physicians. 2011;3(01):037–42.
Colavecchio A, Cadieux B, Lo A, Goodridge LD. Bacteriophages contribute to the spread of antibiotic resistance genes among foodborne pathogens of the Enterobacteriaceae family - A review. Front Microbiol. 2017;8(JUN):1–13.
Talavera-Gonzalez J, Dibarrat J, Reyes Rodriguez NE, Salgado-Miranda C, Talavera-Rojas M. Prevalence of the qnrB, qnrA and blaTEM genes in temperate bacteriophages of Escherichia coli isolated from wastewater and sewer water from slaughterhouses in the State of Mexico. Rev Mex Ciencias Pecu. 2021 Jun 17;
de Mesquita Souza Saraiva M, Lim K, do Monte DFM, Givisiez PEN, Alves LBR, de Freitas Neto OC, et al. Antimicrobial resistance in the globalized food chain: a One Health perspective applied to the poultry industry. Brazilian J Microbiol [Internet]. 2022;53(1):465–86. Available from: https://doi.org/10.1007/s42770-021-00635-8
Monte DF, Lincopan N, Fedorka-Cray PJ, Landgraf M. Current insights on high priority antibiotic-resistant Salmonella enterica in food and foodstuffs: a review. Curr Opin Food Sci [Internet]. 2019;26:35–46. Available from: https://doi.org/10.1016/j.cofs.2019.03.004
Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A. 2015 May;112(18):5649–54.
Hedman HD, Vasco KA, Zhang L. A Review of Antimicrobial Resistance in Poultry Farming within Low-Resource Settings. Anim an open access J from MDPI. 2020 Jul;10(8).
Samreen, Ahmad I, Malak HA, Abulreesh HH. Environmental antimicrobial resistance and its drivers: a potential threat to public health. J Glob Antimicrob Resist [Internet]. 2021;27:101–11. Available from: https://www.sciencedirect.com/science/article/pii/S2213716521001910
Elliott KA, Kenny C, Madan J. A Global Treaty to Reduce Antimicrobial Use in Livestock CGD Policy Paper 102 January 2017. 2017;(January).
Van TTH, Yidana Z, Smooker PM, Coloe PJ. Antibiotic use in food animals worldwide, with a focus on Africa: Pluses and minuses. J Glob Antimicrob Resist [Internet]. 2020;20:170–7. Available from: https://www.sciencedirect.com/science/article/pii/S2213716519301985
Kaur K, Singh S, Kaur R. Impact of antibiotic usage in food-producing animals on food safety and possible antibiotic alternatives. The Microbe [Internet]. 2024;4:100097. Available from: https://www.sciencedirect.com/science/article/pii/S2950194624000645
Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, et al. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother [Internet]. 2004 Jan 1;53(1):28–52. Available from: https://doi.org/10.1093/jac/dkg483
Guo K, Zhao Y, Cui L, Cao Z, Zhang F, Wang X, et al. The Influencing Factors of Bacterial Resistance Related to Livestock Farm: Sources and Mechanisms. Front Anim Sci. 2021;2(September).
S.B. Levy. Factors impacting on the problem of antibiotic resistance. J Antimicrob Chemother. 2002;49:25–30.
Balcázar JL. Implications of bacteriophages on the acquisition and spread of antibiotic resistance in the environment. Int Microbiol. 2020;23(4):475–9.
Meek RW, Vyas H, Jane L, Piddock V. Nonmedical Uses of Antibiotics : Time to Restrict Their Use ? 2015;1–11.
Larsson DGJ, Flach CF. Antibiotic resistance in the environment. Nat Rev Microbiol. 2022 May;20(5):257–69.
Gillieatt BF, Coleman N V. Unravelling the mechanisms of antibiotic and heavy metal resistance co-selection in environmental bacteria. FEMS Microbiol Rev. 2024 Jun;48(4).
Poole K. At the Nexus of Antibiotics and Metals: The Impact of Cu and Zn on Antibiotic Activity and Resistance. Trends Microbiol. 2017 May 1;25.
Zhang Y, Gu AZ, Cen T, Li X, He M, Li D, et al. Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment. Environ Pollut. 2018 Jun;237:74–82.
Deng W, Quan Y, Yang S, Guo L, Zhang X, Liu S, et al. Antibiotic Resistance in Salmonella from Retail Foods of Animal Origin and Its Association with Disinfectant and Heavy Metal Resistance. Microb Drug Resist. 2018;24(6):782–91.
Maillard JY, Bloomfield S, Coelho JR, Collier P, Cookson B, Fanning S, et al. Does microbicide use in consumer products promote antimicrobial resistance? A critical review and recommendations for a cohesive approach to risk assessment. Microb Drug Resist. 2013;19(5):344–54.
Jean-Yves Maillard. Resistance of bacteria to antibiotics. J Pak Med Assoc. 2018;26(4):91–3.
Chukwu KB, Abafe OA, Amoako DG, Essack SY, Abia ALK. Environmental concentrations of antibiotics, biocides, and heavy metals fail to induce phenotypic antimicrobial resistance in Escherichia coli. Sci Total Environ [Internet]. 2023;899(July):165721. Available from: https://doi.org/10.1016/j.scitotenv.2023.165721
Al-Jebouri MM. Impact of Sublethal Disinfectant Exposure on Antibiotic Resistance Patterns of Pseudomonasaeruginosa. Med Princ Pract Int J Kuwait Univ Heal Sci Cent. 2024 Nov;1–7.
Meade E, Slattery MA, Garvey M. Biocidal Resistance in Clinically Relevant Microbial Species: A Major Public Health Risk. Pathog (Basel, Switzerland). 2021 May;10(5).
Zurek L, Ghosh A. Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Appl Environ Microbiol. 2014 Jun;80(12):3562–7.
Raka RN, Zhang L, Chen R, Xue X. Antibiotic Resistance Genes in Global Food Transformation System: Edible Insects vs. Livestock. Vol. 13, Foods. 2024.
Gwenzi W, Chaukura N, Muisa-Zikali N, Teta C, Musvuugwa T, Rzymski P, et al. Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance. Vol. 10, Antibiotics. 2021.
Nayduch D, Neupane S, Pickens V, Purvis T, Olds C. House Flies Are Underappreciated Yet Important Reservoirs and Vectors of Microbial Threats to Animal and Human Health. Microorganisms. 2023 Feb;11(3).
Poudel A, Hathcock T, Butaye P, Kang Y, Price S, Macklin K, et al. Multidrug-resistant Escherichia coli, Klebsiella pneumoniae and Staphylococcus spp. in houseflies and blowflies from farms and their environmental settings. Int J Environ Res Public Health. 2019;16(19):1–12.
Xu Y, Tao S, Hinkle N, Harrison M, Chen J. Salmonella, including antibiotic-resistant Salmonella, from flies captured from cattle farms in Georgia, U.S.A. Sci Total Environ [Internet]. 2018;616–617:90–6. Available from: https://doi.org/10.1016/j.scitotenv.2017.10.324
Sauer K, Stoodley P, Goeres DM, Hall-Stoodley L, Burmølle M, Stewart PS, et al. The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol [Internet]. 2022;20(10):608–20. Available from: https://doi.org/10.1038/s41579-022-00767-0
Michaelis C, Grohmann E. Horizontal Gene Transfer of Antibiotic Resistance Genes in Biofilms. Antibiotics. 2023;12(2).
Aydin A, Suleymanoglu AA, Abdramanov A, Paulsen P, Dumen E. Detection of Extended Spectrum ß-Lactamase-Producing Escherichia coli with Biofilm Formation from Chicken Meat in Istanbul. Foods. 2024;13(7).
Flores-Vargas G, Bergsveinson J, Lawrence JR, Korber DR. Environmental Biofilms as Reservoirs for Antimicrobial Resistance. Front Microbiol. 2021;12(December).
Moawad AA, Hotzel H, Neubauer H, Ehricht R, Monecke S, Tomaso H, et al. Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: Emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli. Gut Pathog [Internet]. 2018;10(1):1–12. Available from: https://doi.org/10.1186/s13099-018-0266-5
Agyare C, Etsiapa Boamah V, Ngofi Zumbi C, Boateng Osei F. Antibiotic Use in Poultry Production and Its Effects on Bacterial Resistance. Antimicrob Resist - A Glob Threat. 2019;
WHO, FAO, WOAH. Technical Brief on Water, Sanitation, Hygiene and Wastewater Management to Prevent Infections and Reduce the Spread of Antimicrobial Resistance. 2020. 32 p.
WHO. Global Antimicrobial Resistance and Use Surveillance System (GLASS) Report 2022. Vol. 33, Braz Dent J. 2022.
CDC. Antibiotic resistance threats in the united states,2019. Cdc. 2019;
Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med [Internet]. 2004;10(12):S122–9. Available from: https://doi.org/10.1038/nm1145
Tilahun M, Kassa Y, Gedefie A, Ashagire M. Emerging Carbapenem-Resistant Enterobacteriaceae Infection, Its Epidemiology and Novel Treatment Options: A Review. Infect Drug Resist. 2021;14:4363–74.
Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N, et al. Antibiotic resistance—the need for global solutions. Lancet Infect Dis [Internet]. 2013 Dec 1;13(12):1057–98. Available from: https://doi.org/10.1016/S1473-3099(13)70318-9
Salam MA, Al-Amin MY, Salam MT, Pawar JS, Akhter N, Rabaan AA, et al. Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Vol. 11, Healthcare. 2023.
Nasri E, Subirats J, Sànchez-Melsió A, Mansour H Ben, Borrego CM, Balcázar JL. Abundance of carbapenemase genes (blaKPC, blaNDM and blaOXA-48) in wastewater effluents from Tunisian hospitals. Environ Pollut [Internet]. 2017;229:371–4. Available from: https://www.sciencedirect.com/science/article/pii/S0269749117307133
Sheu CC, Chang YT, Lin SY, Chen YH, Hsueh PR. Infections Caused by Carbapenem-Resistant Enterobacteriaceae: An Update on Therapeutic Options. Front Microbiol [Internet]. 2019;10. Available from: https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2019.00080
Foster SD. The Economic Burden of Antimicrobial Resistance in the Developing World BT - Antimicrobial Resistance in Developing Countries. In: Sosa A de J, Byarugaba DK, Amábile-Cuevas CF, Hsueh PR, Kariuki S, Okeke IN, editors. New York, NY: Springer New York; 2010. p. 365–84. Available from: https://doi.org/10.1007/978-0-387-89370-9_21
Ikuta KS, Swetschinski LR, Aguilar GR, Sharara F, Mestrovic T, Gray AP, et al. Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2022;400(10369):2221–48.
Laxminarayan R, Van Boeckel T, Frost I, Kariuki S, Khan EA, Limmathurotsakul D, et al. The Lancet Infectious Diseases Commission on antimicrobial resistance: 6 years later. Lancet Infect Dis [Internet]. 2020;20(4):e51–60. Available from: http://dx.doi.org/10.1016/S1473-3099(20)30003-7
Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules. 2018 Mar;23(4).
Odey TOJ, Tanimowo WO, Afolabi KO, Jahid IK, Reuben RC. Antimicrobial use and resistance in food animal production: food safety and associated concerns in Sub-Saharan Africa. Int Microbiol [Internet]. 2024;27(1):1–23. Available from: https://doi.org/10.1007/s10123-023-00462-x
Arsène MMJ, Davares AKL, Viktorovna PI, Andreevna SL, Sarra S, Khelifi I, et al. The public health issue of antibiotic residues in food and feed: Causes, consequences, and potential solutions. Vet World. 2022;15(3):662–71.
Chinemerem Nwobodo D, Ugwu MC, Oliseloke Anie C, Al-Ouqaili MTS, Chinedu Ikem J, Victor Chigozie U, et al. Antibiotic resistance: The challenges and some emerging strategies for tackling a global menace. J Clin Lab Anal. 2022 Sep;36(9):e24655.
Wang Z, Shao C, Shao J, Hao Y, Jin Y. Risk factors of Carbapenem-resistant Enterobacterales intestinal colonization for subsequent infections in hematological patients: a retrospective case-control study. Front Microbiol. 2024;15:1355069.
Dadgostar P. Antimicrobial resistance: implications and costs. Infect Drug Resist. 2019;12:3903–10.
Menz BD, Charani E, Gordon DL, Leather AJM, Moonesinghe SR, Phillips CJ. Surgical Antibiotic Prophylaxis in an Era of Antibiotic Resistance: Common Resistant Bacteria and Wider Considerations for Practice. Infect Drug Resist. 2021;14:5235–52.
Buckley GJ, Palmer GH. Combating Antimicrobial Resistance and Protecting the Miracle of Modern Medicine. Combating Antimicrobial Resistance and Protecting the Miracle of Modern Medicine. 2022. 1–366 p.
AFRICA CDC. Voicing African Priorities on the Active Pandemic. 2024;
Dutescu IA, Hillier SA. Encouraging the Development of New Antibiotics: Are Financial Incentives the Right Way Forward? A Systematic Review and Case Study. Infect Drug Resist. 2021;14:415–34.
Lhermie G, Gröhn YT, Raboisson D. Addressing Antimicrobial Resistance: An Overview of Priority Actions to Prevent Suboptimal Antimicrobial Use in Food-Animal Production. Front Microbiol. 2016;7:2114.
WHO. Antimicrobial Resistance. KEY FACTS. 2021;95(4):405–6.
FAO. Drivers, Dynamics and Epidemiology of antimicrobial resistance in animal production. 2016.
Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T. 2015 Apr;40(4):277–83.
Ibaideya MAT, Taha AA, Qadi M. Phenotypic and molecular characterization of multidrug-resistant Enterobacterales isolated from clinical samples in Palestine : a focus on extended-spectrum β-lactamase- and carbapenemase-producing isolates. 2024;
Singh AK, Kaur R, Verma S, Singh S. Antimicrobials and Antibiotic Resistance Genes in Water Bodies: Pollution, Risk, and Control. Front Environ Sci [Internet]. 2022;10. Available from: https://www.frontiersin.org/journals/environmental-science/articles/10.3389/fenvs.2022.830861
Franklin AM, Weller DL, Durso LM, Bagley M, Davis BC, Frye JG, et al. A one health approach for monitoring antimicrobial resistance: developing a national freshwater pilot effort. Front Water [Internet]. 2024;Volume 6-2024. Available from: https://www.frontiersin.org/journals/water/articles/10.3389/frwa.2024.1359109
Singh S, Kriti M, K.S A, Sharma P, Pal N, Sarma DK, et al. A one health approach addressing poultry-associated antimicrobial resistance: Human, animal and environmental perspectives. The Microbe [Internet]. 2025;7:100309. Available from: https://www.sciencedirect.com/science/article/pii/S2950194625000779
Kalil AC, Metersky ML, Klompas M, Muscedere J, Sweeney DA, Palmer LB, et al. Management of Adults With Hospital-acquired and Ventilator-associated Pneumonia: 2016 Clinical Practice Guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis an Off Publ Infect Dis Soc Am. 2016 Sep;63(5):e61–111.
Ha DR, Haste NM, Gluckstein DP. The Role of Antibiotic Stewardship in Promoting Appropriate Antibiotic Use. Am J Lifestyle Med. 2019;13(4):376–83.
Doron S, Davidson LE. Antimicrobial Stewardship. Mayo Clin Proc [Internet]. 2011 Nov 1;86(11):1113–23. Available from: https://doi.org/10.4065/mcp.2011.0358
Olawade DB, Fapohunda O, Egbon E, Ebiesuwa OA, Usman SO, Faronbi AO, et al. Phage therapy: A targeted approach to overcoming antibiotic resistance. Microb Pathog [Internet]. 2024;197:107088. Available from: https://www.sciencedirect.com/science/article/pii/S0882401024005552
Lin DM, Koskella B, Lin HC. Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther. 2017 Aug;8(3):162–73.
Murugaiyan J, Kumar PA, Rao GS, Iskandar K, Hawser S, Hays JP, et al. Progress in Alternative Strategies to Combat Antimicrobial Resistance: Focus on Antibiotics. Antibiot (Basel, Switzerland). 2022 Feb;11(2).
Mehdi Y, Létourneau-Montminy MP, Gaucher ML, Chorfi Y, Suresh G, Rouissi T, et al. Use of antibiotics in broiler production: Global impacts and alternatives. Anim Nutr [Internet]. 2018;4(2):170–8. Available from: https://www.sciencedirect.com/science/article/pii/S2405654517302512
Millet S, Maertens L. The European ban on antibiotic growth promoters in animal feed: from challenges to opportunities. Vol. 187, Veterinary journal (London, England : 1997). England; 2011. p. 143–4.
Tang KL, Caffrey NP, Nóbrega DB, Cork SC, Ronksley PE, Barkema HW, et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet Heal [Internet]. 2017 Nov 1;1(8):e316–27. Available from: https://doi.org/10.1016/S2542-5196(17)30141-9
Samtiya M, Matthews KR, Dhewa T, Puniya AK. Antimicrobial Resistance in the Food Chain: Trends, Mechanisms, Pathways, and Possible Regulation Strategies. Vol. 11, Foods. 2022.
WHO. Stop using antibiotics in healthy animals to prevent the spread of antibiotic resistance [Internet]. 2017 [cited 2025 Apr 1]. Available from: https://www.who.int/news/item/07-11-2017-stop-using-antibiotics-in-healthy-animals-to-prevent-the-spread-of-antibiotic-resistance
Dikgole T, Christian M, Luvhengo U. FOOD SAFETY KNOWLEDGE AND HANDLING PRACTICES OF POULTRY PRODUCTS BY CONSUMERS IN NGAKA MODIRI MOLEMA DISTRICT, NORTH-WEST PROVINCE. Ponte. 2022 Aug 1;78.