journal article·2024-07-02Open access

Antibiotic Resistance in the Farming Environment

Ewa Karwowska

Applied Sciences· Volume 14· Issue 13

Abstract

Bacterial resistance to antibiotics is now an extremely important safety and health issue. Much of the research on this phenomenon focuses on its clinical aspects, while current findings confirm that it is only one of a number of potential sources of bacteria and genes responsible for drug resistance. There are many indications that one of the main contributors to this issue is currently agriculture and that this applies virtually worldwide. Increased awareness of issues of rational use of antibiotics in husbandry practice entails increased interest in phenomena related to the spread of antibiotic resistance in the environment, their specifics, and the scale of the existing threat. This work, based on current research, analyzed selected aspects of the use of antibiotics in animal production, the presence of antibiotic-resistant microorganisms in farm animals and in waste from agricultural production, in particular from animal breeding farms, the determinants of antibiotic resistance in farming practices and the potential threats related to emissions and spread of antibiotic resistance factors in the environment, including the possibility of transfer of resistant bacteria and resistance genes to humans.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Pharmaceutical and Antibiotic Environmental Impacts · Antibiotic Resistance in Bacteria · Antimicrobial agents and applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Biology, Faculty of Building Services, Hydro and Environmental Engineering, Warsaw University of Technology, Nowowiejska 20, 00-653 Warsaw, Poland

References (100+)

Show source-provided references
1. Serwecińska, L. (2020). Antimicrobials and antibiotic-resistant bacteria: A risk to the environment and to public health. Water, 12.10.3390/w12123313 ↗
2. Existing evidence on antibiotic resistance exposure and transmission to humans from the environment: A systematic map10.1186/s13750-022-00262-2 ↗
3. A review of antibiotic use in food animals: Perspective, policy, and potential10.1177/003335491212700103 ↗
4. Iwu, C.D., Korsten, L., and Okoh, A.I. (2020). The incidence of antibiotic resistance within and beyond the agricultural ecosystem: A concern for public health. Microbiologyopen, 9.10.1002/mbo3.1035 ↗
5. Environmental contamination in a high-income country (France) by antibiotics, antibiotic-resistant bacteria, and antibiotic resistance genes: Status and possible causes10.1016/j.envint.2021.107047 ↗
6. Waglechner, N., and Wright, G.D. (2017). Antibiotic resistance: It’s bad, but why isn’t it worse?. BMC Biol., 15.10.1186/s12915-017-0423-1 ↗
7. Antibiotic resistance genes in the human-impacted environment: A one health perspective10.1016/S1002-0160(18)60062-1 ↗
8. Long-term effect of different fertilization and cropping systems on the soil antibiotic resistome10.1021/acs.est.8b04330 ↗
9. Walsh, F. (2013). Investigating antibiotic resistance in non-clinical environments. Front. Microbiol., 4.10.3389/fmicb.2013.00019 ↗
10. Perceptions of antibiotic use in livestock farming in Germany, Italy and the United States10.1016/j.livsci.2020.104251 ↗
11. Antibiotic stewardship and its implications for agricultural animal-human relationships: Insights from an intensive dairy farm in England10.1016/j.jrurstud.2020.07.008 ↗
12. Consumer perception and understanding of the risks of antibiotic use and antimicrobial resistance in farming10.1007/s10460-022-10399-y ↗
13. Antibiotic resistance in the environment: A critical insight on its occurrence, fate, and eco-toxicity10.1007/s11356-021-13143-x ↗
14. Antibiotic use and resistance in animal farming: A quantitative and qualitative study on knowledge and practices among farmers in Khartoum, Sudan10.1111/j.1863-2378.2012.01458.x ↗
15. Monitoring the perturbation of soil and groundwater microbial communities due to pig production activities10.1128/AEM.03760-12 ↗
16. Skandalis, N., Maeusli, M., Papafotis, D., Miller, S., Lee, B., Theologidis, I., and Luna, B. (2021). Environmental spread of antibiotic resistance. Antibiotics, 10.10.3390/antibiotics10060640 ↗
17. O’Neill, J. (2015). Antimicrobials in Agriculture and the Environment: Reducing Unnecessary Use and Waste: The Review on Antimicrobial Resistance, Wellcometrust.
18. Mitigating antibiotic resistance at the livestock-environment interface: A review10.4014/jmb.1909.09030 ↗
19. Emergence and spread of antibiotic-resistant foodborne pathogens from farm to table10.1007/s10068-022-01157-1 ↗
20. Zalewska, M., Blazejewska, A., Czapko, A., and Popowska, M. (2021). Antibiotics and antibiotic resistance genes in animal manure—Consequences of its application in agriculture. Front. Microbiol., 12.10.3389/fmicb.2021.610656 ↗
21. Antibiotics and antibiotic resistance in agroecosystems: State of the science10.2134/jeq2015.07.0336 ↗
22. Ebmeyer, S., Kristiansson, E., and Larsson, D.J. (2021). A framework for identifying the recent origins of mobile antibiotic resistance genes. Commun. Biol., 4.10.1038/s42003-020-01545-5 ↗
23. A health metadata-based management approach for comparative analysis of high-throughput genetic sequences for quantifying antimicrobial resistance reduction in Canadian hog barns10.1016/j.csbj.2020.09.012 ↗
24. Chekabab, S.M., Lawrence, J.R., Alvarado, A.C., Predicala, B.Z., and Korber, D.R. (2021). Piglet gut and in-barn manure from farms on a raised without antibiotics program display reduced antimicrobial resistance but an increased prevalence of pathogens. Antibiotics, 10.10.3390/antibiotics10101152 ↗
25. Antibiotic resistance and the environment—There and back again. Science & Society series on Science and Drugs10.15252/embr.201438978 ↗
26. Monger, X.C., Gilbert, A.A., Saucier, L., and Vincent, A.T. (2021). Antibiotic resistance: From pig to meat. Antibiotics, 10.10.3390/antibiotics10101209 ↗
27. Patterns of antibiotic use in global pig production: A systematic review10.1016/j.vas.2019.100058 ↗
28. Prophylactic and metaphylactic antimicrobial use in Belgian fattening pig herds10.1016/j.prevetmed.2012.03.001 ↗
29. Wastewater treatment plants as a reservoir of integrase and antibiotic resistance genes—An epidemiological threat to workers and environment10.1016/j.envint.2021.106641 ↗
30. Environmental and public health implications of water reuse: Antibiotics, antibiotic resistant bacteria, and antibiotic resistance genes10.3390/antibiotics2030367 ↗
31. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments10.1038/s41467-018-07992-3 ↗
32. Extended-spectrum βlactamase–producing Enterobacteriaceae among travelers from the Netherlands10.3201/eid1908.130257 ↗
33. Diverse and abundant antibiotic resistance genes in Chinese swine farms10.1073/pnas.1222743110 ↗
34. Tackling antibiotic resistance: The environmental framework10.1038/nrmicro3439 ↗
35. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: Integrating behavioural, epidemiological and One Health approaches10.1098/rspb.2018.0332 ↗
36. Impact factors of the accumulation, migration and spread of antibiotic resistance in the environment10.1007/s10653-020-00759-0 ↗
37. Spread of airborne antibiotic resistance from animal farms to the environment: Dispersal pattern and exposure risk10.1016/j.envint.2021.106927 ↗
38. Antibiotic resistance genes load in an antibiotic free organic broiler farm10.1016/j.psj.2021.101675 ↗
39. Airborne bacterial community and antibiotic resistome in the swine farming environment: Metagenomic insights into livestock relevance, pathogen hosts and public risks10.1016/j.envint.2023.107751 ↗
40. Prevalence of antibiotic resistance in Escherichia coli strains simultaneously isolated from humans, animals, food, and the environment: A systematic review and meta-analysis10.2147/IDR.S201324 ↗
41. Antibiotic resistance in Escherichia coli from farm livestock and related analytical methods: A review10.5740/jaoacint.17-0445 ↗
42. Amador, P., Fernandes, R., Prudencio, C., and Duarte, I. (2019). Prevalence of antibiotic resistance genes in multidrug-resistant Enterobacteriaceae on portuguese livestock manure. Antibiotics, 8.10.3390/antibiotics8010023 ↗
43. Antibiotic resistance of Escherichia coli isolated from poultry and poultry environment of Bangladesh
44. Colonization and antibiotic susceptibility pattern of methicillin resistance Staphylococcus aureus (MRSA) among farm animals in Saudi Arabia
45. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance10.14202/vetworld.2019.984-993 ↗
46. The fecal resistome of dairy cattle is associated with diet during nursing10.1038/s41467-019-12111-x ↗
47. Dairy farm soil presents distinct microbiota and varied prevalence of antibiotic resistance across housing areas10.1016/j.envpol.2019.113058 ↗
48. Tang, M., Zhou, Q., Zhang, X., Zhou, S., Zhang, J., Tang, X., Lu, J., and Gao, Y. (2020). Antibiotic resistance profiles and molecular mechanisms of Campylobacter from chicken and pig in China. Front. Microbiol., 11.10.3389/fmicb.2020.592496 ↗
49. Holmer, I., Salomonsen, C.M., Jorsal, S.E., Astrup, L.B., Jensen, V.F., Hog, B.B., and Pedersen, K. (2019). Antibiotic resistance in porcine pathogenic bacteria and relation to antibiotic usage. BMC Vet. Res., 15.10.1186/s12917-019-2162-8 ↗
50. Differences in antibiotic resistance patterns of Enterococcus faecalis and Enterococcus faecium strains isolated from farm and pet animals10.1128/AAC.45.5.1374-1378.2001 ↗
51. Air exposure as a possible route for ESBL in pig farmers10.1016/j.envres.2017.03.002 ↗
52. Novel antibiotic resistance determinants from agricultural soil exposed to antibiotics widely used in human medicine and animal farming10.1128/AEM.00989-17 ↗
53. Farooq, M., Smoglica, C., Ruffini, F., Soldati, L., Marsilio, F., and Di Francesco, C.E. (2022). Antibiotic Resistance Genes Occurrence in Conventional and Antibiotic-Free Poultry Farming, Italy. Animals, 12.10.3390/ani12182310 ↗
54. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization10.1073/pnas.1409836111 ↗
55. Antimicrobial resistance in bacteria from Swiss veal calves at slaughter10.1111/j.1863-2378.2007.01071.x ↗
56. Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in northwestern Ecuador10.1128/mSphere.00021-15 ↗
57. Österberg, J., Wingstrand, A., Nygaard Jensen, A., Kerouanton, A., Cibin, V., Barco, L., Denis, M., Aabo, S., and Bengtsson, B. (2016). Antibiotic resistance in Escherichia coli from pigs in organic and conventional farming in four European countries. PLoS ONE, 11.10.1371/journal.pone.0157049 ↗
58. Concentrations of antibiotics predicted to select for resistant bacteria: Proposed limits for environmental regulation10.1016/j.envint.2015.10.015 ↗
59. Smalla, K., Cook, K., Djordjevic, S.P., Klümper, U., and Gillings, M. (2018). Environmental dimensions of antibiotic resistance: Assessment of basic science gaps. FEMS Microbiol. Ecol., 94.10.1093/femsec/fiy195 ↗
60. Antibiotic resistance genes in layer farms and their correlation with environmental samples10.1016/j.psj.2021.101485 ↗
61. Lima, T., Domingues, S., and Da Silva, G.J. (2020). Manure as a potential hotspot for antibiotic resistance dissemination by horizontal gene transfer events. Vet. Sci., 7.10.3390/vetsci7030110 ↗
62. Antibiotics and antibiotic resistance from animal manures to soil: A review10.1111/ejss.12494 ↗
63. Bhushan, C., Khurana, A., Sinha, R., and Nagaraju, M. (2017). Antibiotic Resistance in Poultry Environment: Spread of Resistance from Poultry Farm to Agricultural Field, Centre for Science and Environment.
64. Argudin, M., Deplano, A., Meghraoui, A., Dodemont, M., Heinrichs, A., Denis, O., Nonhoff, C., and Roisin, S. (2017). Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics, 6.10.3390/antibiotics6020012 ↗
65. Impact of dairy manure pre-application treatment on manure composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest10.1016/j.scitotenv.2016.12.138 ↗
66. Effect of antibiotic use and composting on antibiotic resistance gene abundance and resistome risks of soils receiving manure-derived amendments10.1016/j.envint.2019.04.043 ↗
67. Antibiotic resistance in the soil ecosystem: A One Health perspective10.1016/j.coesh.2021.100230 ↗
68. Flores-Vargas, G., Bergsveinson, J., Lawrence, J.R., and Korber, D.R. (2021). Environmental biofilms as reservoirs for antimicrobial resistance. Front. Microbiol., 12.10.3389/fmicb.2021.766242 ↗
69. Antibiotic resistance in the environment10.1038/s41579-021-00649-x ↗
70. Fertilizing with animal manure disseminates antibiotic resistance genes to the farm environment10.2134/jeq2015.05.0250 ↗
71. Intensive Poultry Farming Practices Influence Antibiotic Resistance Profiles in Pseudomonas Aeruginosa Inhabiting Nearby Soils10.2147/IDR.S324055 ↗
72. Influence of manure application on the environmental resistome under Finnish agricultural practice with restricted antibiotic use10.1021/acs.est.7b00551 ↗
73. Antimicrobial resistance in dairy slurry tanks: A critical point for measurement and control10.1016/j.envint.2022.107516 ↗
74. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures10.1016/j.soilbio.2018.08.018 ↗
75. Heavy metals, antibiotics and nutrients affect the bacterial community and resistance genes in chicken manure composting and fertilized soil10.1016/j.jenvman.2019.109980 ↗
76. Changes in microbial community structure during pig manure composting and its relationship to the fate of antibiotics and antibiotic resistance genes10.1016/j.jhazmat.2020.122082 ↗
77. Sardar, M.F., Zhu, C., Geng, B., Ahmad, H.R., Song, T., and Li, H. (2021). The fate of antibiotic resistance genes in cow manure composting: Shaped by temperature-controlled composting stages. Bioresour. Technol., 320.10.1016/j.biortech.2020.124403 ↗
78. Composting temperature directly affects the removal of antibiotic resistance genes and mobile genetic elements in livestock manure10.1016/j.envpol.2022.119174 ↗
79. Dynamics of oxytetracycline, sulfamerazine, and ciprofloxacin and related antibiotic resistance genes during swine manure composting10.1016/j.jenvman.2018.09.074 ↗
80. Bioaerosol is an important transmission route of antibiotic resistance genes in pig farms10.1016/j.envint.2021.106559 ↗
81. Antibiotic-resistance genes in waste water10.1016/j.tim.2017.09.005 ↗
82. Horizontal transfer of antibiotic resistance genes in clinical environments10.1139/cjm-2018-0275 ↗
83. Salmonella Persisters Promote the Spread of Antibiotic Resistance Plasmids in the Gut10.1038/s41586-019-1521-8 ↗
84. Nhung, N.T., Chansiripornchai, N., and Carrique-Mas, J.J. (2017). Antimicrobial resistance in bacterial poultry pathogens: A review. Front. Vet. Sci., 4.10.3389/fvets.2017.00126 ↗
85. Importance and implications of antibiotic resistance development in livestock and wildlife farming in South Africa: A Review10.4314/sajas.v48i3.1 ↗
86. Assessing the risk of antibiotic resistance transmission from the environment to humans: Non-direct proportionality between abundance and risk10.1016/j.tim.2016.11.014 ↗
87. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria10.1038/ismej.2007.31 ↗
88. Balcázar, J.L., Subirats, J., and Borrego, C.M. (2015). The role of biofilms as environmental reservoirs of antibiotic resistance. Front. Microbiol., 6.10.3389/fmicb.2015.01216 ↗
89. Environmental stress and antibiotic resistance in food-related pathogens10.1128/AEM.00578-06 ↗
90. Seiler, C., and Berendonk, T.U. (2012). Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol., 3.10.3389/fmicb.2012.00399 ↗
91. Heavy metal pollution promotes antibiotic resistance potential in the aquatic environment10.1016/j.envpol.2021.116569 ↗
92. Giacometti, F., Shirzad-Aski, H., and Ferreira, S. (2021). Antimicrobials and food-related stresses as selective factors for antibiotic resistance along the farm to fork continuum. Antibiotics, 10.10.3390/antibiotics10060671 ↗
93. Agrichemicals and antibiotics in combination increase antibiotic resistance evolution10.7717/peerj.5801 ↗
94. Metagenomic analysis of bacterial and viral assemblages from a freshwater creek and irrigated field reveals temporal and spatial dynamics10.1016/j.scitotenv.2019.135395 ↗
95. Raw wastewater irrigation for urban agriculture in three African cities increases the abundance of transferable antibiotic resistance genes in soil, including those encoding extended spectrum betalactamases (ESBLs)10.1016/j.scitotenv.2019.134201 ↗
96. Wang, G., Li, G., Chang, J., Kong, Y., Jiang, T., Wang, J., and Yuan, J. (2021). Enrichment of antibiotic resistance genes after sheep manure aerobic heap composting. Bioresour. Technol., 323.10.1016/j.biortech.2020.124620 ↗
97. The potential implications of reclaimed wastewater reuse for irrigation on the agricultural environment: The knowns and unknowns of the fate of antibiotics and antibiotic resistant bacteria and resistance genes–a review10.1016/j.watres.2017.07.004 ↗
98. Fahrenfeld, N.L., Ma, Y., O’Brien, M., and Pruden, A. (2013). Reclaimed water as a reservoir of antibiotic resistance genes: Distribution system and irrigation implications. Front. Microbiol., 4.10.3389/fmicb.2013.00130 ↗
99. Impact of treated wastewater irrigation on antibiotic resistance in the soil microbiome10.1007/s11356-013-1505-4 ↗
100. Airborne transmission as an integral environmental dimension of antimicrobial resistance through the “One Health” lens10.1080/10643389.2021.2006537 ↗