Important antibiotics in human medicine have been used for many decades in animal agriculture for growth promotion and disease treatment. Several publications have linked antibiotic resistance development and spread with animal production. Aquaculture, the newest and fastest growing food production sector, may promote similar or new resistance mechanisms. This review of 650+ papers from diverse sources examines parallels and differences between land-based agriculture of swine, beef, and poultry and aquaculture. Among three key findings was, first, that of 51 antibiotics commonly used in aquaculture and agriculture, 39 (or 76%) are also of importance in human medicine; furthermore, six classes of antibiotics commonly used in both agriculture and aquaculture are also included on the World Health Organization’s (WHO) list of critically important/highly important/important antimicrobials. Second, various zoonotic pathogens isolated from meat and seafood were observed to feature resistance to multiple antibiotics on the WHO list, irrespective of their origin in either agriculture or aquaculture. Third, the data show that resistant bacteria isolated from both aquaculture and agriculture share the same resistance mechanisms, indicating that aquaculture is contributing to the same resistance issues established by terrestrial agriculture. More transparency in data collection and reporting is needed so the risks and benefits of antibiotic usage can be adequately assessed.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Davies J. Where have all the antibiotics gone? Can J Infect Dis Med Microbiol. 2006;17(5):287.
Zhang L, Kinkelaar D, Huang Y, Li Y, Li X, Wang HH. Acquired antibiotic resistance: are we born with it? Appl Environ Microbiol. 2011;77(89):7134–41.
Nikaido H. Multidrug resistance in bacteria. Annu Rev Biochem. 2009;78:119–46.
WHO. Antimicrobial Resistance—Global Report on Surveillance. World Health Organization. 2014. http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf. Accessed 24 Nov 2014.
Mathew AG, Cissell R, Liamthong S. Antibiotic resistance in bacteria associated with food animals: a United States perspective of livestock production. Foodborne Pathog Dis. 2007;4(89):115–33.
EU. Ban on antibiotics as growth promoters in animal feed enters into effect. European Union. 2005. http://europa.eu/rapid/press-release_IP-05-1687_en.htm. Accessed 24 Nov 2014.
Pruden A, Larsson DGJ, Amezquita A, Collignon P, Brandt KK, Graham DW, et al. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect. 2013;121(8):878–85.
Cabello FC. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol. 2006;8(7):1137–44.
Silbergeld EK, Graham J, Price LB. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health. 2008;29:151–69.
Rasheed MU, Thajuddin N, Ahamed P, Teklemariam Z, Jamil K. Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Rev Inst Med Trop Sao Paulo. 2014;56(89):341–6.
Ta YT, Nguyen TT, To PB, Pham DX, Le HTH, Thi GN, et al. Quantification, serovars, and antibiotic resistance of Salmonella isolated from retail raw chicken meat in Vietnam. J Food Prot. 2014;77(89):57–66.
Asadpour L. Antibacterial drug resistance patterns in poultry isolated enterococci. Afr J Microbiol Res. 2012;6(29):5857–61.
Hsu JT, Chen CY, Young CW, Chao WL, Li MH, Liu YH, et al. Prevalence of sulfonamide-resistant bacteria, resistance genes and integron-associated horizontal gene transfer in natural water bodies and soils adjacent to a swine feedlot in northern Taiwan. J Hazard Mater. 2014;277:34–43.
Li L, Sun J, Liu BT, Zhao DH, Ma J, Deng H, et al. Quantification of lincomycin resistance genes associated with lincomycin residues in waters and soils adjacent to representative swine farms in China. Front Microbiol. 2013;4:364.
Knapp CW, Dolfing J, Ehlert PAI, Graham DW. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol. 2010;44(89):580–7.
Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, et al. Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int. 2008;34(8):1215–26.
Shah SQA, Cabello FC, L'Abee-Lund TM, Tomova A, Godfrey HP, Buschmann AH, et al. Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites. Environ Microbiol. 2014;16(5):1310–20.
Ryu SH, Park SG, Choi SM, Hwang YO, Ham HJ, Kim SU, et al. Antimicrobial resistance and resistance genes in Escherichia coli strains isolated from commercial fish and seafood. Int J Food Microbiol. 2012;152(1–2):14–8.
CVM. 2011 Retail Meat Report. National Antimicrobial Resistance Monitoring System. Center for Veterinary Medicine, Food and Drug Administration. 2011. http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/ucm059103.htm. Accessed 24 Nov 2014.
USDA. Production, supply and distribution online. United States Department of Agriculture. Foreign Agricultural Service. 2014. http://apps.fas.usda.gov/psdonline/. Accessed 4 August 2014.
FAO. FAOSTAT. Food and Agricultural Organization of the United Nations. 2014. http://www.faostat.fao.org. Accessed 24 Nov 2014.
FAO. The state of world fisheries and aquaculture, 2012. Food and Agriculture Organization of the United Nations. Rome, Italy. 2012. http://www.fao.org/docrep/016/i2727e/i2727e.pdf. Accessed 24 Nov 2014.
Cole DW, Cole R, Gaydos SJ, Gray J, Hyland G, Jacques ML, et al. Aquaculture: environmental, toxicological, and health issues. Int J Hyg Environ Health. 2009;212(89):369–77.
Rico A, Satapornvanit K, Haque MM, Min J, Nguyen PT, Telfer TC, et al. Use of chemicals and biological products in Asian aquaculture and their potential environmental risks: a critical review. Rev Aquac. 2012;4(89):75–93.
FAO. FishStat fishery statistical collections: aquaculture production (1950–2008). Food and Agricultural Organization of the United Nations, Rome. 2010. http://www.fao.org/fishery/topic/16073/en. Accessed 24 Nov 2014.
Buschmann AH, Cabello F, Young K, Carvajal J, Varela DA, Henriquez L. Salmon aquaculture and coastal ecosystem health in Chile: analysis of regulations, environmental impacts and bioremediation systems. Ocean Coast Manag. 2009;52(5):243–9.
FDA. 2011 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals. Center for Veterinary Medicine. 2011. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM338170.pdf. Accessed 24 Nov 2014.
EMA. European Medicine Agency. European surveillance of veterinary antimicrobial consumption, 2013. “Sales of Veterinary Antimicrobials in 25 EU/EEA Countries in 2011” (EMA/236501/2013). 2011. http://www.ema.europa.eu/docs/en_GB/document_library/Report/2013/10/WC500152311.pdf. Accessed 24 Nov 2014.
Ganguly NK, Arora NK, Chandy SJ, Fairoze MN, Gill JPS, Gupta U, et al. Rationalizing antibiotic use to limit antibiotic resistance in India. Indian J Med Res. 2011;134(3):281–94.
NICD. National Policy for Containment of Antimicrobial Resistance India 2011. National Centre for Disease Control, Directorate General of Health Services, Ministry of Health and Family Welfare Nirman Bhawan, New Delhi. 2011. http://nicd.nic.in/ab_policy.pdf. Accessed 24 Nov 2014.
Zhao L, Dong YH, Wang H. Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ. 2010;408(5):1069–75.
Chen YS, Zhang HB, Luo YM, Song J. Occurrence and dissipation of veterinary antibiotics in two typical swine wastewater treatment systems in east China. Environ Monit Assess. 2012;184(89):2205–17.
Regitano JB, Leal RMP. Performance and environmental impact of antibiotics in animal production in Brazil. Rev Bras Cienc Solo. 2010;34(3):601–16.
Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011;24(89):718–33.
Chapman HD, Jeffers TK, Williams RB. Forty years of monensin for the control of coccidiosis in poultry. Poult Sci. 2010;89(9):1788–801.
Coffman J. The use of drugs in food animals: benefits and risks: CAB International; 1999.
Maron DF, Smith TJS, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Globalization and Health. 2013;9(48).
FDA. #213 Guidance for Industry. US Department of Health and Human Services Food and Drug Administration Center for Veterinary Medicine. 2013. http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM299624.pdf. Accessed 25 Sep 2014 .
Sarmah AK, Meyer MT, Boxall ABA. A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere. 2006;65(5):725–59.
Broughton EI, Walker DG. Policies and practices for aquaculture food safety in China. Food Policy. 2010;35(5):471–8.
Jin S. Regulation, realities and recommendation on antimicrobial use in food animal production in China. In: the Medical Impact of the Use of Antimicrobials in Food Animals. WHO, Geneva (Section 2.3.4). 1997.
Hu XG, Zhou QX, Luo Y. Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut. 2010;158(9):2992–8.
Alday-Sanz V, Corsin F, Irde E, Bondad-Reantaso MG. Survey on the use of veterinary medicines in aquaculture. In M.G. Bondad-Reantaso, J.R. Arthur & R.P. Subasinghe, eds. Improving biosecurity through prudent and responsible use of veterinary medicines in aquatic food production, pp. 29–44. FAO Fisheries and Aquaculture Technical Paper No. 547. Rome, FAO, 207 pp. 2012.
WHO. Critically important antimicrobials for human medicine. 3rd Revision 2011. World Health Organization. Geneva, Switzerland. 2012. http://apps.who.int/iris/bitstream/10665/77376/1/9789241504485_eng.pdf. Accessed 26 Sep 2014.
WHO. Critically important antimicrobials for human medicine: categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use. Report of the Second WHO Expert Meeting. 2007;Copenhage, 29–31 May 2007. http://www.who.int/foodborne_disease/resistance/antimicrobials_human.pdf. Accessed 24 Nov 2014.
Hao HH, Cheng GY, Iqbal Z, Ai XH, Hussain HI, Huang LL, et al. Benefits and risks of antimicrobial use in food-producing animals. Frontiers in Microbiology. 2014;5(288).
Kemper N. Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic. 2008;8(89):1–13.
Yuan X, Chen W. Use of Veterinary Medicines in Chinese Aquaculture: Current Status. In M.G. Bondad-Reantaso, J.R. Arthur and R.P. Subasinghe, eds. Improving Biosecurity Through Prudent and Responsible Use of Veterinary Medicines in Aquatic Food Production, pp. 51–67. FAO Fisheries and Aquaculture Technical Paper No 547. 2012 (Rome, FAO. 207 pp.).
Mor-Mur M, Yuste J. Emerging bacterial pathogens in meat and poultry: an overview. Food Bioproc Technol. 2010;3(89):24–35.
Feldhusen F. The role of seafood in bacterial foodborne diseases. Microb Infect. 2000;2(13):1651–60.
Herrera FC, Santos JA, Otero A, Garcia-Lopez ML. Occurrence of foodborne pathogenic bacteria in retail prepackaged portions of marine fish in Spain. J Appl Microbiol. 2006;100(3):527–36.
Normanno G, Parisi A, Addante N, Quaglia NC, Dambrosio A, Montagna C, et al. Vibrio parahaemolyticus, Vibrio vulnificus and microorganisms of fecal origin in mussels (Mytilus galloprovincialis) sold in the Puglia region (Italy). Int J Food Microbiol. 2006;106(89):219–22.
Novotny L, Dvorska L, Lorencova A, Beran V, Pavlik I. Fish: a potential source of bacterial pathogens for human beings. Vet Med. 2004;49(9):343–58.
Sapkota AR, Lefferts LY, McKenzie S, Walker P. What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. Environ Health Perspect. 2007;115(5):663–70.
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. 2004;53(89):28–52.
Mellon M, Benbrook C, Benbrook KL. Hogging It. Estimates of Antimicrobial Abuse in Livestock. Union of Concerned Scientists Cambridge, MA. 2001. http://www.ucsusa.org/assets/documents/food_and_agriculture/hog_front.pdf. Accessed 4 August 2014.
Butaye P, Devriese LA, Haesebrouck F. Antimicrobial growth promoters used in animal feed: Effects of less well known antibiotics on gram-positive bacteria. Clin Microbiol Rev. 2003;16(89):175–88.
Graham JP, Boland JJ, Silbergeld E. Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep. 2007;122(89):79–87.
Marti E, Variatza E, Balcazar JL. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol. 2014;22(89):36–41.
Baquero F, Martinez JL, Canton R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol. 2008;19(3):260–5.
Zounkova R, Kliemesova Z, Nepejchalova L, Hilscherova K, Blaha L. Complex evaluation of toxicity and genotoxicity of antimicrobials oxytetracycline and flumequine used in aquaculture. Environ Toxicol Chem. 2011;30(5):1184–9.
Park S, Choi K. Hazard assessment of commonly used agricultural antibiotics on aquatic ecosystems. Ecotoxicology. 2008;17(6):526–38.
Giedraitiene A, Vitkauskiene A, Naginiene R, Pavilonis A. Antibiotic resistance mechanisms of clinically important bacteria. Med Lith. 2011;47(3):137–46.
Nikaido H, Pages J-M. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol Rev. 2012;36(89):340–63.
Uddin GMN, Larsen MH, Guardabassi L, Dalsgaard A. Bacterial flora and antimicrobial resistance in raw frozen cultured seafood imported to Denmark. J Food Prot. 2013;76(3):490–9.
Chen S, Zhao SH, White DG, Schroeder CM, Lu R, Yang HC, et al. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol. 2004;70(1):1–7.
Meng HC, Zhang ZG, Chen MR, Su YY, Li L, Miyoshi S, et al. Characterization and horizontal transfer of class 1 integrons in Salmonella strains isolated from food products of animal origin. Int J Food Microbiol. 2011;149(3):274–7.
Van TTH, Moutafis G, Tran LT, Coloe PJ. Antibiotic resistance in food-borne bacterial contaminants in Vietnam. Appl Environ Microbiol. 2007;73(24):7906–11.
Jiang XB, Shi L. Distribution of tetracycline and trimethoprim/sulfamethoxazole resistance genes in aerobic bacteria isolated from cooked meat products in Guangzhou, China. Food Control. 2013;30(1):30–4.
Nawaz M, Khan SA, Tran Q, Sung K, Khan AA, Adamu I, et al. Isolation and characterization of multidrug-resistant Klebsiella spp. isolated from shrimp imported from Thailand. Int J Food Microbiol. 2012;155(3):179–84.
Done HY, Halden RU. Reconnaissance of 47 antibiotics and associated microbial risks in seafood sold in the United States. J Hazard Mater. 2015;282:10–7.
Koo HJ, Woo GJ. Distribution and transferability of tetracycline resistance determinants in Escherichia coli isolated from meat and meat products. Int J Food Microbiol. 2011;145(2–3):407–13.
Tadesse DA, Bahnson PB, Funk JA, Morrow WEM, Abley MJ, Ponte VA, et al. Yersinia enterocolitica of porcine origin: carriage of virulence genes and genotypic diversity. Foodborne Pathog Dis. 2013;10(89):80–6.
Food and Water Watch. Factory Farm Map. Food and Water Watch. 2007. http://www.factoryfarmmap.org. Accessed 24 Nov 2014.
Department of Agriculture. Census of Aquaculture Publication. “Freshwater and Saltwater Acres Used for Aquaculture Production, by State and United States: 2005 and 1998”. United States Department of Agriculture. 2005. http://www.agcensus.usda.gov/Publications/2002/Aquaculture/. Accessed 24 Nov 2014.
NOAA. U.S. Commercial Fishery Landings. Commercial Fisheries Statistics. National Oceanic and Atmospheric Administration. 2012. http://www.st.nmfs.noaa.gov/commercial-fisheries/fus/fus12/. Accessed 24 Nov 2014.
NOAA. Aquaculture in the United States. National Oceanic and Atmospheric Administration Fisheries. 2014. http://www.nmfs.noaa.gov/aquaculture/aquaculture_in_us.html. Accessed 24 Nov 2014.
NOAA. In the U.S. FishWatch U.S. Seafood Facts. National Oceanic and Atmospheric Administration. 2014. http://www.fishwatch.gov/farmed_seafood/in_the_us.htm. Accessed 24 Nov 2014.
USDA. Top 10 States. 2005 Census of Aquaculture. US Department of Agriculture, the Census of Agriculture. Last updated 2007. 2005. http://www.agcensus.usda.gov/Publications/2002/Aquaculture/index4.asp. Accessed 24 Nov 2014.
FDA. Drug Use Review. Department of Health and Human Services, Public Health Service, Food and Drug Administration, Center for Drug Evaluation and Research, Office of Surveillance and Epidemiology. April 5, 2012. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM338170.pdf. Accessed 24 Nov 2014.
NRDC. Food, Farm animals, and Drugs. Natural Resources Defense Council. 2014. http://www.nrdc.org/food/saving-antibiotics.asp. Accessed 4 Aug 2014.
DeWaal CG, Grooters SV. Antibiotic Resistance Foodborne Pathogens. Center for Science in the Public Interest White Paper. Washington, DC. 2013. http://cspinet.org/new/pdf/outbreaks_antibiotic_resistance_in_foodborne_pathogens_2013.pdf. Accessed 24 Nov 2014.
USFRA. Food Source: Antibiotics. The Food Dialogues. U.S. Farmers and Ranchers Association. 2007. http://www.fooddialogues.com/foodsource/antibiotics. Accessed 24 Nov 2014.
FDA. 2009 Summary Report on antimicrobials sold or distributed for use in food-producing animals Food and Drug Administration, Department of Health and Human Services: Center for Veterinary Medicine. 2010. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM231851.pdf. Accessed 24 Nov 2014.
Slaughter L. Confirmed: 80 Percent of all Antibacterial Drugs Used on Animals, Endangering Human Health. Congresswoman Louise M Slaughter. 2011. http://louise.house.gov/press-releases/confirmed-80-percent-of-all-antibacterial-drugs-used-on-animals-endangering-human-health/. Accessed 24 Nov 2014.
MacDonald JM, Wang SL. Foregoing sub-therapeutic antibiotics: the impact on broiler grow-out operations. Appl Econ Perspect Policy. 2011;33(89):79–98.
FDA. #209. Guidance for Industry. The Judicious Use of Medically Important Antimicrobial Drugs in Food-Producing Animals. US Department of Health and Human Services Food and Drug Administration Center for Veterinary Medicine. 2012. http://www.fda.gov/downloads/animalveterinary/guidancecomplianceenforcement/guidanceforindustry/ucm216936.pdf. Accessed 25 Sep 2014.
Benbrook CM. Antibiotic Drug Use in US Aquaculture. Northwest Science and Environmental Policy Center Sandpoint, Idaho. 2002. http://www.iatp.org/documents/antibiotic-drug-use-in-us-aquaculture-1. Accessed 24 November 2014.
NOAA. Feeds for Aquaculture. National Oceanic and Atmospheric Administration Fisheries. 2014. http://www.nmfs.noaa.gov/aquaculture/faqs/faq_feeds.html. Accessed 24 Nov 2014.
FDA. Approved Drugs. United States Food and Drug Administration US Department of Health and Human Services. 2014. http://www.fda.gov/animalveterinary/developmentapprovalprocess/aquaculture/ucm132954.htm. Accessed 24 Nov 2014.
Rakowski KT. Thermal inactivation of Escherichia coil O157:H7 and Salmonella on catfish and tilapia. Food Microbiol. 2012;30(89):427–31.
Powell JL. Vibrio species. Clin Lab Med. 1999;19(3):537–52.
Williams TC, Ayrapetyan M, Oliver JD. Implications of chitin attachment for the environmental persistence and clinical nature of the human pathogen Vibrio vulnificus. Appl Environ Microbiol. 2014;80(5):1580–7.
Reynaud Y, Pitchford S, De Decker S, Wikfors GH, Brown CL. Molecular Typing of Environmental and Clinical Strains of Vibrio vulnificus Isolated in the Northeastern USA. Plos One. 2013;8(12).
Turner JW, Paranjpye RN, Landis ED, Biryukov SV, Gonzalez-Escalona N, Nilsson WB, et al. Population Structure of Clinical and Environmental Vibrio parahaemolyticus from the Pacific Northwest Coast of the United States. Plos One. 2013;8(89).
Givens CE, Bowers JC, DePaola A, Hollibaugh JT, Jones JL. Occurrence and distribution of Vibrio vulnificus and Vibrio parahaemolyticus—potential roles for fish, oyster, sediment and water. Lett Appl Microbiol. 2014;58(6):503–10.
Heinitz ML, Ruble RD, Wagner DE, Tatini SR. Incidence of Salmonella in fish and seafood. J Food Prot. 2000;63(5):579–92.
Amagliani G, Brandi G, Schiavano GF. Incidence and role of Salmonella in seafood safety. Food Res Int. 2012;45(89):780–8.
The authors would like to thank Patty Lovera of the Food and Water Watch for graciously letting us use the density maps for US agriculture of cattle, swine, and poultry. We would also like to thank Diane Windham, Kevin Amos, and Barbara Seekins of NOAA for providing resources and email correspondences regarding US aquaculture antibiotic usage and census data. Thanks to Mae Wu of the NRDC, Margaret Mellon (Science Policy Consultant), David Love (Johns Hopkins University), Keeve Nachman (Johns Hopkins University), and Steve Roach (Food Animals Concerns Trust) for their communications and help with antibiotics usage data and references. This study was supported in part by the Piper Charitable Trust and by the National Institute of Environmental Health Sciences grants R01ES015445, R01ES020889 and their respective supplements. The content of this work is solely the responsibility of the authors and does not necessarily represent the official views of the NIEHS or the National Institutes of Health (NIH).
Guest Editors: James P. Laurenson, Raanan A. Bloom, and Nakissa Sadrieh
ELECTRONIC SUPPLEMENTARY MATERIAL
Below is the link to the electronic supplementary material.
(DOCX 206 kb)
About this article
Cite this article
Done, H.Y., Venkatesan, A.K. & Halden, R.U. Does the Recent Growth of Aquaculture Create Antibiotic Resistance Threats Different from those Associated with Land Animal Production in Agriculture?. AAPS J 17, 513–524 (2015). https://doi.org/10.1208/s12248-015-9722-z