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Cited by 451Antibiotic Use and ResistanceAntibiotic Resistance in BacteriaPharmaceutical and Antibiotic Environmental Impacts

Antibiotic use in food animals worldwide, with a focus on Africa: Pluses and minuses

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Van, Thi Thu Hao, Yidana, Zuwera, Smooker, Peter M., Coloe, Peter J.·2020·Journal of Global Antimicrobial Resistance
DOI 10.1016/j.jgar.2019.07.031
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Abstract

Antibiotics are frequently used in food animal production in developing countries to promote the well-being and growth of animals. This practice provides some economic benefits to producers and consumers at large. Nevertheless, this practice is also associated with a number of concerns. A major concern has been that repeatedly exposing these animals to small doses of antibiotics contributes significantly to antimicrobial resistance, since a good fraction of the antibiotics used are the same or surrogates of antibiotics used in human therapeutic practices. Studies over decades have shown an explicit relationship between antimicrobial use and antimicrobial resistance in veterinary science. Many antibiotics can be purchased over the counter in African countries, and antibiotic resistance is an important issue to address in this region. This review examines some of the risks and benefits associated with antibiotic use in food animals. We conclude that the use of antibiotics in food animal production constitutes a major contributing factor to the current antimicrobial resistance crisis and that antibiotics should only be used for the treatment of sick animals based on prior diagnosis of disease.

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  • The rapid emergence of antimicrobial-resistant pathogens is often accelerated by the inappropriate use and overuse of antimicrobial agents, especially antibiotics, in humans, animals, and agriculture or the environment.

    “Indeed, the rapid emergence of antimicrobial-resistant pathogens is often accelerated by the inappropriate use and overuse of antimicrobial agents, especially antibiotics, in humans, animals, and agriculture/the environment.”

    From Antimicrobial Resistance Rates and Surveillance in Sub-Saharan Africa: Where Are We Now? (2022) · cites this paper as [19]

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  1. Cully M. Public health: the politics of antibiotics. Nature 2014;509:S16-7, doi: http://dx.doi.org/10.1038/509S16a. · DOI
  2. Rushton J. Anti-microbial use in animals: how to assess the trade-offs. Zoonoses Public Health 2015;62(Suppl. 1):10-21, doi:http://dx.doi.org/ 10.1111/zph.12193. · DOI
  3. Finley RL, Collignon P, Larsson DG, McEwen SA, Li XZ, Gaze WH, et al. The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 2013;57:704-10, doi:http://dx.doi.org/10.1093/cid/cit355. · DOI · Paper page
  4. Durso LM, Cook KL. Impacts of antibiotic use in agriculture: what are the benefits and risks? Curr Opin Microbiol 2014;19:37-44, doi:http://dx.doi. org/10.1016/j.mib.2014.05.019. · DOI
  5. Littmann J, Viens AM. The ethical significance of antimicrobial resistance. Public Health Ethics 2015;8:209-24, doi:http://dx.doi.org/10.1093/phe/phv025. · DOI
  6. Littmann J, Buyx A, Cars O. Antibiotic resistance: an ethical challenge. Int J Antimicrob Agents 2015;46:359-61, doi:http://dx.doi.org/10.1016/j.ijantimi- cag.2015.06.010. · DOI
  7. Founou LL, Founou RC, Essack SY. Antibiotic resistance in the food chain: a developing country-perspective. Front Microbiol 2016;7:1881, doi:http://dx. doi.org/10.3389/fmicb.2016.01881. · DOI
  8. Eagar H, Swan G, van Vuuren M. A survey of antimicrobial usage in animals in South Africa with specific reference to food animals. J S Afr Vet Assoc 2012;83:16, doi:http://dx.doi.org/10.4102/jsava.v83i1.16. · DOI
  9. Woolhouse M, Ward M, van Bunnik B, Farrar J. Antimicrobial resistance in humans, livestock and the wider environment. Philos Trans R Soc Lond Ser B Biol Sci 2015;370:20140083, doi:http://dx.doi.org/10.1098/rstb.2014.0083. · DOI
  10. Argudín MA, Deplano A, Meghraoui A, Dodémont M, Heinrichs A, Denis O, et al. Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics (Basel) 2017;6:E12, doi:http://dx.doi.org/10.3390/antibiot- ics6020012. · DOI
  11. 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;112:5649-54, doi:http://dx.doi.org/10.1073/pnas.1503141112. · DOI
  12. Boamah VE, Agyare C, Odoi H, Dalsgaard A. Practices and factors influencing the use of antibiotics in selected poultry farms in Ghana. J Antimicro 2016;2:120.
  13. McEwen SA, Fedorka-Cray PJ. Antimicrobial use and resistance in animals. Clin Infect Dis 2002;34(Suppl 3):S93-106, doi:http://dx.doi.org/10.1086/ 340246. · DOI
  14. Lekshmi M, Ammini P, Kumar S, Varela MF. The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms 2017;5:E11, doi:http://dx.doi.org/10.3390/ microorganisms5010011. · DOI · Paper page
  15. Chantziaras I, Boyen F, Callens B, Dewulf J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J Antimicrob Chemother 2014;69:827-34, doi: http://dx.doi.org/10.1093/jac/dkt443. · DOI
  16. Cogliani C, Goossens H, Greko C. Restricting antimicrobial use in food animals: lessons from Europe: banning nonessential antibiotic uses in food animals is intended to reduce pools of resistance genes. Microbe 2011;6:274- 9, doi:http://dx.doi.org/10.1128/microbe.6.274.1. · DOI
  17. Maron DF, Smith TJ, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Global Health 2013;9:48, doi:http://dx.doi.org/10.1186/1744-8603-9-48. · DOI
  18. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis 2013;13:1057-98, doi:http://dx.doi.org/10.1016/S1473-3099(13)70318-9. · DOI · Paper page
  19. Allen HK. Antibiotic resistance gene discovery in food-producing animals. Curr Opin Microbiol 2014;19:25-9, doi:http://dx.doi.org/10.1016/j.mib.2014.06.001. · DOI
  20. Doumith M, Godbole G, Ashton P, Larkin L, Dallman T, Day M, et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother 2016;71:2300-5, doi:http://dx.doi.org/ 10.1093/jac/dkw093. · DOI
  21. Gustafson RH, Bowen RE. Antibiotic use in animal agriculture. J Appl Microbiol 1997;83:531-41, doi:http://dx.doi.org/10.1046/j.1365-2672.1997.00280.x. · DOI
  22. Murnane D. A preliminary report on the treatment of clinical and subclinical streptococcal and staphylococcal infections of the bovine udder with penicillin. Aust Vet J 1945;21:82-90, doi:http://dx.doi.org/10.1111/j.1751- 0813.1945.tb06422.x. · DOI
  23. De Briyne N, Atkinson J, Pokludová L, Borriello SP. Antibiotics used most commonly to treat animals in Europe. Vet Rec 2014;175:325, doi:http://dx. doi.org/10.1136/vr.102462. · DOI
  24. Gilchrist MJ, Greko C, Wallinga DB, Beran GW, Riley DG, Thorne PS. The potential role of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance. Environ Health Perspect 2007;115:313- 6, doi:http://dx.doi.org/10.1289/ehp.8837. · DOI
  25. Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP. Antibiotics in agriculture and the risk to human health: how worried should we be? Evol Appl 2015;8:240-7, doi:http://dx.doi.org/10.1111/eva.12185. · DOI
  26. Collignon PC, Conly JM, Andremont A, McEwen SA, Aidara-Kane A, Agerso Y, et al. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis 2016;63:1087-93, doi:http://dx.doi.org/10.1093/ cid/ciw475. · DOI
  27. Adesokan HK, Akanbi IO, Akanbi IM, Obaweda RA. Pattern of antimicrobial usage in livestock animals in south-western Nigeria: the need for alternative plans. Onderstepoort J Vet Res 2015;82:816, doi:http://dx.doi.org/10.4102/ ojvr.v82i1.816. · DOI
  28. Donkor ES, Newman MJ, Yeboah-Manu D. Epidemiological aspects of non- human antibiotic usage and resistance: implications for the control of antibiotic resistance in Ghana. Trop Med Int Health 2012;17:462-8, doi: http://dx.doi.org/10.1111/j.1365-3156.2012.02955.x. · DOI
  29. Manishimwe R, Nishimwe K, Ojok L. Assessment of antibiotic use in farm animals in Rwanda. Trop Anim Health Prod 2017;49:1101-6, doi:http://dx. doi.org/10.1007/s11250-017-1290-z. · DOI
  30. Alonso CA, Zarazaga M, Ben Sallem R, Jouini A, Ben Slama K, Torres C. Antibiotic resistance in Escherichia coli in husbandry animals: the African perspective. Lett Appl Microbiol 2017;64:318-34, doi:http://dx.doi.org/ 10.1111/lam.12724. · DOI
  31. Dibner JJ, Richards JD. Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 2005;84:634-43, doi:http://dx.doi.org/ 10.1093/ps/84.4.634. · DOI
  32. Mensah SE, Koudandé OD, Sanders P, Laurentie M, Mensah GA, Abiola FA. Antimicrobial residues in foods of animal origin in Africa: public health risks. Rev Sci Tech 2014;33:987-96.
  33. Salama NA, Abou-Raya SH, Shalaby AR, Emam WH, Mehaya FM. Incidence of tetracycline residues in chicken meat and liver retailed to consumers. Food Addit Contam Part B Surveill 2011;4:88-93, doi:http://dx.doi.org/10.1080/ 19393210.2011.585245. · DOI
  34. Jukes TH, Williams WL. Nutritional effects of antibiotics. Pharmacol Rev 1953;5:381-420.
  35. Heuer H, Schmitt H, Smalla K. Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 2011;14:236- 43, doi:http://dx.doi.org/10.1016/j.mib.2011.04.009. · DOI · Paper page
  36. Bengtsson B, Greco C. Antibiotic resistance-consequences for animal health, welfare, and food production. Ups J Med Sci 2014;119:96-102, doi:http://dx. doi.org/10.3109/03009734.2014.901445. · DOI
  37. Witte W. Medical consequences of antibiotic use in agriculture. Science 1998;279:996-7, doi:http://dx.doi.org/10.1126/science.279.5353.996. · DOI · Paper page
  38. Li D, Yu T, Zhang Y, Yang M, Li Z, Liu M, et al. Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Appl Environ Microbiol 2010;76:3444-51, doi:http://dx.doi.org/10.1128/AEM.02964-09. · DOI
  39. Ma L, Li B, Zhang T. Abundant rifampin resistance genes and significant correlations of antibiotic resistance genes and plasmids in various environ- ments revealed by metagenomic analysis. Appl Microbiol Biotechnol 2014;98:5195-204, doi:http://dx.doi.org/10.1007/s00253-014-5511-3. · DOI
  40. Langdon A, Crook N, Dantas G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med 2016;8:39, doi:http://dx.doi.org/10.1186/ s13073-016-0294-z. · DOI
  41. Ince D, Hooper DC. Quinolone resistance due to reduced target enzyme expression. J Bacteriol 2003;185:6883-92, doi:http://dx.doi.org/10.1128/ JB.185.23.6883-6892.2003. · DOI
  42. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 2006;12:83-8, doi:http://dx. doi.org/10.1038/nm1347. · DOI
  43. Li XZ, Nikaido H. Efflux-mediated drug resistance in bacteria: an update. Drugs 2009;69:1555-623, doi:http://dx.doi.org/10.2165/11317030- 000000000-00000. · DOI
  44. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DJ. Co-occurrence of resistance genes to antibiotics, biocides and metals reveal novel insights into their co-selection potential. BMC Genomics 2015;16:964, doi:http://dx.doi. org/10.1186/s12864-015-2153-5. · DOI
  45. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 2016;16:161-8, doi:http://dx.doi.org/10.1016/S1473-3099 (15)00424-7. · DOI
  46. Malhotra-Kumar S, Xavier BB, Das AJ, Lammens C, Hoang HT, Pham NT, et al. Colistin-resistant Escherichia coli harbouring mcr-1 isolated from food animals in Hanoi, Vietnam. Lancet Infect Dis 2016;16:286-7, doi:http://dx. doi.org/10.1016/S1473-3099(16)00014-1. · DOI
  47. Hasman H, Hammerum AM, Hansen F, Hendriksen RS, Olesen B, Agersø Y, et al. Detection of mcr-1 encoding plasmid-mediated colistin-resistant Escherichia coli isolates from human bloodstream infection and imported chicken meat, Denmark 2015. Euro Surveill 2015;20:, doi:http://dx.doi.org/ 10.2807/1560-7917.ES.2015.20.49.30085. · DOI
  48. Grami R, Mansour W, Mehri W, Bouallègue O, Boujaâfar N, Madec JY, et al. Impact of food animal trade on the spread of mcr-1-mediated colistin resistance, Tunisia, July 2015. Euro Surveill 2016;21:30144, doi:http://dx.doi. org/10.2807/1560-7917.ES.2016.21.8.30144. · DOI
  49. Morrill HJ, Pogue JM, Kaye KS, LaPlante KL. Treatment options for carbapenem-resistant Enterobacteriaceae infections. Open Forum Infect Dis 2015;2:ofv050, doi:http://dx.doi.org/10.1093/ofid/ofv050. · DOI
  50. Olaitan AO, Chabou S, Okdah L, Morand S, Rolain JM. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 2016;16:147, doi:http://dx. doi.org/10.1016/S1473-3099(15)00540-X. · DOI
  51. Perreten V, Strauss C, Collaud A, Gerber D. Colistin resistance gene mcr-1 in avian-pathogenic Escherichia coli in South Africa. Antimicrob Agents Chemother 2016;60:4414-5, doi:http://dx.doi.org/10.1128/AAC.00548-16. · DOI
  52. Osei Sekyere J. Current state of resistance to antibiotics of last-resort in South Africa: a review from a public health perspective. Front Public Health 2016;4:209, doi:http://dx.doi.org/10.3389/fpubh.2016.00209. · DOI
  53. Kluytmans J. Plasmid-encoded colistin resistance: mcr-one, two, three and counting. Euro Surveill 2017;22:pii: 30588, doi:http://dx.doi.org/10.2807/ 1560-7917.ES.2017.22.31.30588. · DOI
  54. Carattoli A, Villa L, Feudi C, Curcio L, Orsini S, Luppi A, et al. Novel plasmid- mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill 2017;22:pii: 30589, doi:http://dx.doi.org/10.2807/1560-7917.ES.2017.22.31.30589. · DOI
  55. Borowiak M, Fischer J, Hammerl JA, Hendriksen RS, Szabo I, Malorny B. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in D-tartrate ferment- ing Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother 2017;72:3317-24, doi:http://dx.doi.org/10.1093/jac/dkx327. · DOI
  56. Carroll LM, Gaballa A, Guldimann C, Sullivan G, Henderson LO, Wiedmann M. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype Typhi- murium isolate. MBio 2019;10:, doi:http://dx.doi.org/10.1128/mBio.00853- 19 pii: e00853-00819. · DOI · Paper page
  57. Donovan C. If FDA does not regulate food, who will? A study of hormones and antibiotics in meat production. Am J Law Med 2015;41:459-82, doi:http://dx. doi.org/10.1177/0098858815591528. · DOI
  58. Shah M, Kathiiko C, Wada A, Odoyo E, Bundi M, Miringu G, et al. Prevalence, seasonal variation, and antibiotic resistance pattern of enteric bacterial pathogens among hospitalized diarrheic children in suburban regions of central Kenya. Trop Med Health 2016;44:39, doi:http://dx.doi.org/10.1186/ s41182-016-0038-1. · DOI
  59. Ndihokubwayo JB, Yahaya AA, Dester AT, Ki-Zerbo G, Odei EA, Keita B, et al. Antimicrobial resistance in the African region: issues, challenges and actions proposed. African Health Monitor 2013;16:27-30.
  60. Wirth T. Massive lineage replacements and cryptic outbreaks of Salmonella Typhi in eastern and southern Africa. Nat Genet 2015;47:565-7, doi:http:// dx.doi.org/10.1038/ng.3318. · DOI
  61. Leopold SJ, van Leth F, Tarekegn H, Schultsz C. Antimicrobial drug resistance among clinically relevant bacterial isolates in sub-Saharan Africa: a systematic review. J Antimicrob Chemother 2014;69:2337-53, doi:http:// dx.doi.org/10.1093/jac/dku176. · DOI
  62. Jans C, Merz A, Johler S, Younan M, Tanner SA, Kaindi DW, et al. East and West African milk products are reservoirs for human and livestock-associated Staphylococcus aureus. Food Microbiol 2017;65:64-73, doi:http://dx.doi.org/ 10.1016/j.fm.2017.01.017. · DOI
  63. Zishiri OT, Mkhize N, Mukaratirwa S. Prevalence of virulence and antimicrobial resistance genes in Salmonella spp. isolated from commercial chickens and human clinical isolates from South Africa and Brazil. Onderstepoort J Vet Res 2016;83:a1067, doi:http://dx.doi.org/10.4102/ojvr. v83i1.1067. · DOI
  64. Ateba CN, Bezuidenhout CC. Characterisation of Escherichia coli O157 strains from humans, cattle and pigs in the North-West Province, South Africa. Int J Food Microbiol 2008;128:181-8, doi:http://dx.doi.org/10.1016/j.ijfoodmi- cro.2008.08.011. · DOI
  65. Beyi AF, Fite AT, Tora E, Tafese A, Genu T, Kaba T, et al. Prevalence and antimicrobial susceptibility of Escherichia coli O157 in beef at butcher shops and restaurants in central Ethiopia. BMC Microbiol 2017;17:49, doi:http://dx. doi.org/10.1186/s12866-017-0964-z. · DOI
  66. Asiimwe BB, Baldan R, Trovato A, Cirillo DM. Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pastoral communities of South-West Uganda. BMC Infect Dis 2017;17:422, doi:http:// dx.doi.org/10.1186/s12879-017-2524-4. · DOI
  67. Schaumburg F, Alabi AS, Peters G, Becker K. New epidemiology of Staphylococcus aureus infection in Africa. Clin Microbiol Infect 2014;20:589-96, doi:http://dx.doi.org/10.1111/1469-0691.12690. · DOI
  68. Abdi RD, Mengstie F, Beyi AF, Beyene T, Waktole H, Mammo B. Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC Infect Dis 2017;17:352, doi:http://dx.doi.org/10.1186/s12879-017-2437-2. · DOI
  69. Ed-Dra A, Filali FR, Karraouan B, El Allaoui A, Aboulkacem A, Bouchrif B. Prevalence, molecular and antimicrobial resistance of Salmonella isolated from sausages in Meknes, Morocco. Microb Pathog 2017;105:340-5, doi: http://dx.doi.org/10.1016/j.micpath.2017.02.042. · DOI
  70. Amajoud N, Bouchrif B, El Maadoudi M, Skalli Senhaji N, Karraouan B, El Harsal A, et al. Prevalence, serotype distribution, and antimicrobial resistance of Salmonella isolated from food products in Morocco. J Infect Dev Ctries 2017;11:136-42, doi:http://dx.doi.org/10.3855/jidc.8026. · DOI
  71. Iwu CJ, Iweriebor BC, Obi LC, Basson AK, Okoh AI. Multidrug-resistant Salmonella isolates from swine in the Eastern Cape Province, South Africa. J Food Prot 2016;79:1234-9, doi:http://dx.doi.org/10.4315/0362-028X.JFP-15-224. · DOI
  72. Andoh LA, Dalsgaard A, Obiri-Danso K, Newman MJ, Barco L, Olsen JE. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect 2016;144:3288-99, doi:http://dx.doi.org/ 10.1017/S0950268816001126. · DOI · Paper page
  73. Elmadiena MM, El Hussein AA, Muckle CA, Cole L, Wilkie E, Mistry K, et al. Antimicrobial susceptibility and multi-drug resistance of Salmonella enterica subspecies enterica serovars in Sudan. Trop Anim Health Prod 2013;45:1113- 8, doi:http://dx.doi.org/10.1007/s11250-012-0334-7. · DOI
  74. Shilangale RP, Di Giannatale E, Chimwamurombe PM, Kaaya GP. Prevalence and antimicrobial resistance pattern of Salmonella in animal feed produced in Namibia. Vet Ital 2012;48:125-32.
  75. Dione MM, Geerts S, Antonio M. Characterisation of novel strains of multiply antibiotic-resistant Salmonella recovered from poultry in Southern Senegal. J Infect Dev Ctries 2012;6:436-42, doi:http://dx.doi.org/10.3855/jidc.1530. · DOI
  76. Sibhat B, Molla Zewde B, Zerihun A, Muckle A, Cole L, Boerlin P, et al. Salmonella serovars and antimicrobial resistance profiles in beef cattle, slaughterhouse personnel and slaughterhouse environment in Ethiopia. Zoonoses Public Health 2011;58:102-9, doi:http://dx.doi.org/10.1111/j.1863- 2378.2009.01305.x. · DOI
  77. Abbassi-Ghozzi I, Jaouani A, Hammami S, Martinez-Urtaza J, Boudabous A, Gtari M. Molecular analysis and antimicrobial resistance of Salmonella isolates recovered from raw meat marketed in the area of' Grand Tunis', Tunisia. Pathol Biol (Paris) 2012;60:e49-54, doi:http://dx.doi.org/10.1016/j. patbio.2011.07.005. · DOI
  78. Mezali L, Hamdi TM. Prevalence and antimicrobial resistance of Salmonella isolated from meat and meat products in Algiers (Algeria). Foodborne Pathog Dis 2012;9:522-9, doi:http://dx.doi.org/10.1089/fpd.2011.1032. · DOI
  79. Cabello FC, Godfrey HP, Tomova A, Ivanova L, Dölz H, Millanao A, et al. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Environ Microbiol 2013;15:1917-42, doi:http://dx.doi.org/10.1111/1462-2920.12134. · DOI
  80. Ghosh S, LaPara TM. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 2007;1:191-203, doi:http://dx.doi.org/10.1038/ ismej.2007.31. · DOI
  81. Marti E, Variatza E, Balcazar JL. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol 2014;22:36-41, doi:http://dx.doi.org/ 10.1016/j.tim.2013.11.001. · DOI
  82. Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, et al. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 2013;13:155-65, doi:http://dx.doi. org/10.1016/S1473-3099(12)70317-1. · DOI
  83. Ballard DP, Peterson EA, Nadler JL, Khardori NM. Antibiotic use in animal feed and its impact on antibiotic resistance in human pathogens. In: Khardori N, editor. Food microbiology: in human health and disease. CRC Press; 2015. p. 137-55.
  84. Agga GE, Arthur TM, Durso LM, Harhay DM, Schmidt JW. Antimicrobial- resistant bacterial populations and antimicrobial resistance genes obtained from environments impacted by livestock and municipal waste. PLoS One 2015;10:e0132586, doi:http://dx.doi.org/10.1371/journal.pone.0132586. · DOI
  85. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, et al. In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci U S A 2012;109:1691-6, doi:http://dx.doi.org/10.1073/pnas.1120238109. · DOI · Paper page
  86. Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM, Male MJ, et al. Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS One 2013;8: e63704, doi:http://dx.doi.org/10.1371/journal.pone.0063704. · DOI
  87. Liu J, Zhao Z, Orfe L, Subbiah M, Call DR. Soil-borne reservoirs of antibiotic- resistant bacteria are established following therapeutic treatment of dairy calves. Environ Microbiol 2016;18:557-64, doi:http://dx.doi.org/10.1111/ 1462-2920.13097. · DOI
  88. Tasho RP, Cho JY. Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: a review. Sci Total Environ 2016;563-564:366-76, doi: http://dx.doi.org/10.1016/j.scitotenv.2016.04.140. · DOI
  89. Zhang T, Li B. Occurrence, transformation, and fate of antibiotics in municipal wastewater treatment plants. Crit Rev Environ Sci Technol 2011;41:951-98, doi:http://dx.doi.org/10.1080/10643380903392692. · DOI
  90. Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 2014;12:465-78, doi:http://dx.doi.org/ 10.1038/nrmicro3270. · DOI
  91. Tello A, Austin B, Telfer TC. Selective pressure of antibiotic pollution on bacteria of importance to public health. Environ Health Perspect 2012;120:1100-6, doi:http://dx.doi.org/10.1289/ehp.1104650. · DOI · Paper page
  92. Sidrach-Cardona R, Hijosa-Valsero M, Marti E, Balcázar JL, Becares E. Prevalence of antibiotic-resistant fecal bacteria in a river impacted by both an antibiotic production plant and urban treated discharges. Sci Total Environ 2014;488-489:220-7, doi:http://dx.doi.org/10.1016/j.scitotenv.2014.04.100. · DOI
  93. Van TT, Nguyen HN, Smooker PM, Coloe PJ. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food- producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 2012;154:98-106, doi:http://dx.doi.org/10.1016/j.ijfoodmi- cro.2011.12.032. · DOI
  94. Kirk MD, Angulo FJ, Havelaar AH, Black RE. Diarrhoeal disease in children due to contaminated food. Bull World Health Organ 2017;95:233-4, doi:http:// dx.doi.org/10.2471/BLT.16.173229. · DOI · Paper page
  95. Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014;2014:827965, doi:http://dx.doi.org/10.1155/2014/827965. · DOI
  96. Cheng G, Hao H, Xie S, Wang X, Dai M, Huang L, et al. Antibiotic alternatives: the substitution of antibiotics in animal husbandry? Front Microbiol 2014;5:217, doi:http://dx.doi.org/10.3389/fmicb.2014.00217. · DOI
  97. Reid G, Friendship R. Alternatives to antibiotic use: probiotics for the gut. Anim Biotechnol 2002;13:97-112, doi:http://dx.doi.org/10.1081/ABIO- 120005773. · DOI
  98. Allen HK, Trachsel J, Looft T, Casey TA. Finding alternatives to antibiotics. Ann N Y Acad Sci 2014;1323:91-100, doi:http://dx.doi.org/10.1111/nyas.12468. · DOI
  99. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci 2003;82:627-31, doi:http://dx.doi.org/10.1093/ ps/82.4.627. · DOI
  100. Musa HH, Wu SL, Zhu CH, Seri HI, Zhu GQ. The potential benefits of probiotics in animal production and health. J Anim Vet Adv 2009;8:313-21.
  101. Aminov R, Caplin J, Chanishvili N, Coffey A, Cooper I, De Vos D, et al. Application of bacteriophages. Microbiol Aust 2017;38:63-6.
  102. Ben Lagha A, Haas B, Gottschalk M, Grenier D. Antimicrobial potential of bacteriocins in poultry and swine production. Vet Res 2017;48:22, doi:http:// dx.doi.org/10.1186/s13567-017-0425-6. · DOI
  103. Kumar M, Kumar V, Roy D, Kushwaha R, Vaiswani S. Application of herbal feed additives in animal nutrition-a review. Int J Livest Res 2014;4:1-8, doi: http://dx.doi.org/10.5455/ijlr.20141205105218. · DOI
  104. Murugesan GR, Syed B, Hander S, Pender C. Phytogenic feed additives as an alternative to antibiotic growth promoters in broiler chickens. Front Vet Sci 2015;2:21, doi:http://dx.doi.org/10.3389/fvets.2015.00021. · DOI
  105. Ricke SC. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult Sci 2003;82:632-9, doi:http://dx.doi.org/10.1093/ps/ 82.4.632. · DOI
  106. Bragg R, van der Westhuizen W, Lee JY, Coetsee E, Boucher C. Bacteriophages as potential treatment option for antibiotic resistant bacteria. Adv Exp Med Biol 2014;807:97-110, doi:http://dx.doi.org/10.1007/978-81-322-1777-0_7. · DOI
  107. Wernicki A, Nowaczek A, Urban-Chmiel R. Bacteriophage therapy to combat bacterial infections in poultry. Virol J 2017;14:179, doi:http://dx.doi.org/ 10.1186/s12985-017-0849-7. · DOI
  108. Verstappen KM, Tulinski P, Duim B, Fluit AC, Carney J, van Nes A, et al. The effectiveness of bacteriophages against methicillin-resistant Staphylococcus aureus ST398 nasal colonization in pigs. PLoS One 2016;11:e0160242, doi: http://dx.doi.org/10.1371/journal.pone.0160242. · DOI
  109. Allen HK, Levine UY, Looft T, Bandrick M, Casey TA. Treatment, promotion, commotion: antibiotic alternatives in food-producing animals. Trends Microbiol 2013;21:114-9, doi:http://dx.doi.org/10.1016/j.tim.2012.11.001. · DOI
  110. Riber U, Heegaard PM, Cordes H, Ståhl M, Jensen TK, Jungersen G. Vaccination of pigs with attenuated Lawsonia intracellularis induced acute phase protein responses and primed cell-mediated immunity without reduction in bacterial shedding after challenge. Vaccine 2015;33:156-62, doi:http://dx. doi.org/10.1016/j.vaccine.2014.10.084. · DOI
  111. Alderton MR, Fahey KJ, Coloe PJ. Humoral responses and salmonellosis protection in chickens given a vitamin-dependent Salmonella typhimurium mutant. Avian Dis 1991;35:435-42, doi:http://dx.doi.org/10.2307/1591205. · DOI
  112. Hernández-Jover M, Higgins V, Bryant M, Rast L, McShane C. Biosecurity and the management of emergency animal disease among commercial beef producers in New South Wales and Queensland (Australia). Prev Vet Med 2016;134:92-102, doi:http://dx.doi.org/10.1016/j.prevetmed.2016.10.005. · DOI

Cited by

Sorted by citations

Authors
Van, T. T. H., Yidana, Z., Smooker, P. M., & Coloe, P. J.
Affiliations
  • RMIT University (AU)
  • Kintampo Health Research Centre (GH)
Corresponding author
Smooker, Peter M.
ORCID
Venue
Journal of Global Antimicrobial Resistance
Publisher
Elsevier BV
Published
2020-03
Volume
20
Pages
170-177
ISSN
2213-7165 (ISSN-L)
DOI
10.1016/j.jgar.2019.07.031
OpenAlex
W2967844082
Cited by
451
References
0
Citations by year
2026: 49 · 2025: 84 · 2024: 96 · 2023: 58 · 2022: 83 · 2021: 61 · 2020: 19 · 2013: 1
FWCI
4.56
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Global Antimicrobial Resistance (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • RMIT Research Repository (RMIT University Library) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion)
Topics
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
Keywords
antimicrobial resistance, veterinary antibiotics, food animal production, developing countries, Africa, over-the-counter antibiotics, growth promoters, antibiotic stewardship
MeSH terms
Africa, Animals, Animal Feed, Anti-Bacterial Agents, Food Microbiology, Humans, Drug Resistance, Bacterial

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