Antibiotic Resistance, Alternatives, and the U.S. Poultry Industry
Antimicrobial resistance (AMR) is a global public health issue with important implications in the U.S. For years, antibiotics and antimicrobial compounds have widely been used across the U.S. poultry industry to treat and prevent disease threats and to promote growth (Chapman and Johnson, 2002; Sneeringer et al., 2015).
The connection between antimicrobial use and selection for AMR has been extensively studied, as reported by Hedman et al. (2020). Within the U.S., 80 percent of antimicrobial agents produced are applied to animal production (Food and Drug Administration, 2019). Intensive animal food production can lead to resistance resulting from extended use of antibiotics for promoting growth, preventing disease, and treating infection (Laxminarayan et al., 2013; Silbergeld et al., 2010; You & Silbergeld, 2014).
Antibiotic Usage Decreasing
Even though AMR genes occur naturally (Durso et al., 2012), agricultural practices can influence the prevalence and occurrence of AMR genes in soils. For example, soil applications of swine manure increased erythromycin resistance gene abundance that remained high for a decade post-application (Scott et al., 2018). Today, the poultry industry is keenly aware of the antimicrobial resistance issue, and there is widespread, ongoing research targeting safe and effective antibiotic alternatives.
Antibiotic use in the poultry industry is not a recent phenomenon. The discovery that antimicrobials fed in subtherapeutic concentrations to poultry expedited their growth was accidental. The first use of antibiotics in poultry was reported in nutritional studies by Moore et al. (1946). This was soon followed by the first report of antibiotic resistance in food animals (turkeys) by Starr and Reynolds (1951).
However, several FDA reports over the past 25 years have documented decreased antibiotic use by the U.S. poultry industry. For example, in a survey from 1995 to 2000, there was a substantial decrease in the use of antibiotics by the broiler industry (FDA, 2014). However, a 2011 report estimated that 20 to 52 percent of broiler operations used antibiotics for production purposes not related to disease control (USDA, 2011). But this report also found a long-term decline in antibiotic use in broiler production (Sneeringer et al., 2015).
More recently, FDA (2017) reported that domestic sales and distribution of all medically important antimicrobials intended for use in food-producing animals decreased by 33 percent between 2016 and 2017. The U.S. Poultry and Egg Association (2019) reported a decrease in the percentage of broiler chicks that received hatchery antibiotics from 93 percent in 2013 to 17 percent in 2017, a 95 percent drop in in-feed tetracycline use in broiler chickens, a 67 percent reduction in in-feed tetracycline use in turkeys, and a 42 percent drop in hatchery use of gentamicin in turkey poults. In addition, Poultry Health Today (2020) reported broilers raised in “no antibiotics ever” (NAE) systems accounted for 58 percent of total U.S. production in 2019, a seven-point increase over the previous 12 months.
While there has been discussion on the links between antibiotic use in animal production and human health (Vaughn and Copeland, 2004), perhaps the greatest contributing factor to the recent decline in antibiotic use in livestock is the demand by consumers for NAE poultry products. These demands have occurred even though NAE products often cost more to produce and consumers are often unwilling to pay the increased cost. However, there is growing consumer interest in sustainable food production and knowing how food is raised. As a result, current research is devoted to identifying antibiotic alternatives that can support sustainable bird growth and defend against disease threats (Sneeringer et al., 2015; Gadde et al., 2017). This has led to the broiler industry taking the lead in livestock production systems that have as their mission to meet consumer demands and be “no antibiotics ever.”
Poultry Litter Management
A major issue today for growers, researchers, and the entire poultry industry is the area of poultry litter management. The U.S. is the world’s largest poultry producer, with more than 9 billion broilers produced in 2019; roughly 58 percent of broilers are produced in five southeastern states (Georgia, Arkansas, Alabama, North Carolina, and Mississippi; National Chicken Council, 2020). Poultry litter is a combination of bedding material (shavings, sawdust, rice hulls, etc.), manure, wasted feed, and feathers.
The amount of litter produced by broiler chickens is significant. A 20,000-bird broiler house will produce approximately 150 tons of litter per year (Ritz and Merka, 2013). Therefore, in areas of concentrated poultry production, large volumes of poultry litter are produced in relatively small geographic areas. While this litter can serve as a valuable source of nutrients, it may also be a possible source of AMR bacterial populations in the environment (Thanner et al., 2016).
Some estimates indicate that nearly 14 million tons of poultry litter is produced on U.S. broiler farms annually (Moore et al., 1995; Gollehon et al., 2001). Poultry litter-amended soil may serve as a non-point source for antibiotics that enter surface and ground waters via runoff and leaching (Yang et al., 2019), because approximately 30 to 80 percent of veterinary antibiotics administered to animals are excreted in manure and urine (Sarmah et al., 2006).
Many antimicrobial compounds we use in animal healthcare today were originally isolated from the soil (Yang et al., 2019). This is not surprising considering that soils are a large reservoir of microbial diversity. In fact, 1 gram of soil may contain 106 to 109 bacterial cells from 103 to 106 different bacterial species (Girvan et al., 2003; Torsvik, 2002). Furthermore, antibiotic-resistant genes are not a new occurrence.
Antimicrobial-resistant genes have been recovered from 30,000-year-old permafrost samples, indicating AMR is an ancient phenomenon that existed long before antibiotic usage became common (D’Costa et al., 2011). Therefore, even though it has been suggested that there is a relationship between antibiotic use in agricultural animals and AMR emergence, it is not the only explanation for AMR prevalence (Yang et al., 2019). Administration of antibiotics to agricultural animals is only one possible explanation for AMR.
Approaches for Decreasing AMR
There is concern that land application of poultry litter may transport AMR microorganisms to the environment outside the poultry house. However, there are currently several approaches being undertaken by poultry operations to address AMR. These include multidisciplinary strategies aimed at developing new drugs, antibiotic alternatives, and management practices (FDA, 2013), along with reducing total antibiotic use, as discussed previously. Of these various approaches, developing new drugs is likely the least promising. Only a small handful of new antibiotics have been approved since the 1960s (Butler and Buss, 2006) because developing new antimicrobial drugs is extremely labor intensive, time consuming, and costly.
Research surrounding antibiotic alternatives is proving more promising. Society is pressing for reduced antibiotic use and greater efforts to find effective alternatives to control infectious diseases on farms (Gadde et al., 2017). In response to this pressure, several classes of antibiotic alternatives have been proposed and tested in poultry production, including probiotics, prebiotics, symbiotics, organic acids, enzymes, plant extracts, metals, antibacterial vaccines, immunomodulatory agents, antimicrobial peptides, bacteriophages, and different broiler chicken growth systems (Montoro-Dasi et al., 2020).
The most popular of these alternatives currently appear to be probiotics, prebiotics, and a variety of plant extracts, which are in various research trials aimed at finding antibiotic alternatives that provide both growth promotion and microorganism defense benefits. Prebiotics, such as fructans and galactans, and more recently, dietary fibers (Ricke, 2015, 2018) are selectively used by host microorganisms to confer a health benefit (Gibson et al., 2017). Probiotics such as Bifidobacterium, Bacillus, Lactobacillus, and Lactococcus are live microorganisms that confer a health benefit on the host (World Health Organization, 2011).
Plant extracts are plant-derived compounds that represent a relatively safe, effective, and environmentally friendly source of antimicrobials despite their sometimes-inconsistent nature. In other words, research sometimes finds an encouraging response, and other times, it doesn’t. However, plant extracts have been used for many years in numerous different cultures as food preservatives and dietary supplements to reduce spoilage and promote growth. Products currently being researched include coconut oil, cinnamon, thyme, oregano, clove oil, pine oil, and others.
Despite the research, much remains unknown about how management practices may affect AMR—not only poultry litter management, but also pasture management and grazing practices after poultry litter is land applied. The ability of pasture management practices (i.e., filter strips and continuous versus rotational grazing) to reduce AMR gene sequence, prevalence, and movement to soils is largely unknown (Yang et al., 2020). Yang et al. (2020) reported that poultry litter had lower abundance of AMR genes relative to cattle manure, although long-term applications of poultry litter on pastures increased the abundance of AMR genes in soil. However, indications were that conservation pasture management practices and select poultry litter inputs may minimize the presence and abundance of AMR genes in grassland soils.
In addition, the poultry industry is researching a variety of management practices that address AMR but also have an added welfare component. Practices such as reduced stocking densities, additional downtime between flocks, and investigating slow-growing broilers are aimed at lessening the need for antimicrobial interventions while providing an improved animal-welfare environment.
Summary
Much remains unknown concerning antibiotic resistance and its connection with the U.S. poultry industry. However, something we do know is that antibiotic resistance has been ongoing for thousands of years. As a result, AMR genes are ubiquitous and represent a huge reservoir of genetic material that we can potentially affect with production practices and management efforts related to poultry litter and grass and croplands. A better understanding of soil and poultry litter and the role each plays in the creation of antibiotic-resistant genes will allow the poultry industry to better address antimicrobial resistance. Additional research on antibiotic alternatives such as prebiotics, enzymes, probiotics, organic acids, and plant extracts could provide new tools for the poultry industry to meet consumer demand for NAE products. As the poultry industry strives for increasingly sustainable production practices, careful evaluation of antibiotic use should lessen or prevent further dissemination of antimicrobial resistance.
References
Butler, M. S., and A. D. Buss. 2006. Natural products: The future scaffolds for novel antibiotics? Biochem. Pharmacol. 71:919–929.
Chapman, H. D., and Z. B. Johnson. 2002. Use of antibiotics and roxarsone in broiler chickens in the USA: Analysis of the years 1995 to 2000. Poult. Sci. 81:356–364.
D’Costa, V. M., C. E. King, L. Kalan, M. Morar, C. Schwarz, et al. 2011. Antibiotic resistance is ancient. Nature. 477:457–461. Available at: https://www.nature.com/articles/nature10388. Accessed: November 10, 2020.
Durso, L. M., D. A. Wedin, J. E. Gilley, D. N. Miller, and D. B. Marx. 2016. Assessment of selected antibiotic resistances in ungrazed native Nebraska Prairie soils. J. Environ. Qual. 45:454–462.
Food and Drug Administration (FDA). 2013. Food and Drug Administration, Center for Veterinary Medicine Guidance for Industry #213. Available at: https://www.fda.gov/media/83488/download. Accessed: November 9, 2020.
Food and Drug Administration (FDA). 2014. NARMS Integrated Report: 2014. The National Antimicrobial Resistance Monitoring System (NARMS): Enteric Bacteria. Silver Spring, MD. US FDA. 33 pages. Available at: https://www.fda.gov/media/101511/download. Accessed: November 10, 2020.
Food and Drug Administration (FDA). 2017. Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals. Available at: https://www.fda.gov/animal-veterinary/cvm-updates/fda-releases-annual-summary-report-antimicrobials-sold-or-distributed-2017-use-food-producing#:~:text=The%202017%20Summary%20Report%20on,year%20of%20reported%20sales%20in. Accessed: November 10, 2020.
Food and Drug Administration (FDA). 2019. 2018 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals. Available at: https://www.fda.gov/media/133411/download. Accessed: November 11, 2020.
Gadde, U., W. Kim, S. Oh, and H. Lillehoj. 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: A review. Anim. Health Res. Rev. 18:26–35.
Gibson, G. R., R. Hutkins, M. E. Sanders, et al. 2017. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol Hepatol. 14:491–502.
Girvan, M. S., J. Bullimore, J. N. Pretty, A. M. Osborn, and A. S. Ball. 2003. Soil type is the primary determinant of the composition of the total and active bacterial communities in Arable soils. Appl. Environ. Microbiol. 69:1800–1809.
Gollehon, N., M. Casewell, M. Ribaudo, et al. 2001. Confined animal production and manure nutrients. Agricultural Information Bulletin No. 771, USDA-ERS, Washington, D.C.
Hedman, H. D., K. A. Vasco, and L. Zhang. 2020. A review of antimicrobial resistance in poultry farming within low-resource settings. Animals 10, 1264. doi:10.3390/ani10081264.
Laxminarayan, R., A. Duse, C. Wattal, et al. 2013. Antibiotic resistance: The need for global solutions. Lancet Infect. Dis. 13:1057–1098.
Montoro-Dias, L., A. Villagra, S. Sevilla-Navarro, et al. 2020. The dynamic of antibiotic resistance in commensal Escherichia coli throughout the growing period in broiler chickens: Fast-growing vs. slow-growing breeds. Poult. Sci. 99:1591–1597.
Moore, P. A., T. C. Daniel Jr., A. N. Sharpley, and C. W. Wood. 1995. Poultry manure management: Environmentally sound options. J. Soil Water Cons. 50: 321–327.
Moore, P. R., A. Evenson, T. D. Luckey, et al. 1946. Use of sulfasuxidine, strepothricin, and streptomycin in nutritional studies with the chick. J. Biol. Chem. 165:437–441.
National Chicken Council. 2020. Top broiler producing states. Available at: https://www.nationalchickencouncil.org/about-the-industry/statistics/top-broiler-producing-states/. Accessed: November 6, 2020.
Poultry Health Today. 2020. Nearly 60% of US broilers now raised without antibiotics, but that number may have peaked. Available at: https://poultryhealthtoday.com/nearly-60-of-us-broilers-now-raised-without-antibiotics-but-that-number-may-have-peaked/?utm_source=Poultry+Health+Today+Newsletter&utm_campaign=daab24c737-AAAP_antimicrobial_stewardship_PHT_1_8_2018_COPY_0&utm_medium=email&utm_term=0_5ac605299a-daab24c737-315439401. Accessed: November 5, 2020.
Ricke, S. C. 2015. Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems. Poult. Sci. 94:1411–1418.
Ricke, S. C. 2018. Impact of prebiotics on poultry production and food safety. Yale J. Biol. Med. 91:151–159.
Ritz, C. W., and W. C. Merka. 2013. Maximizing poultry litter manure use through nutrient management planning. University of Georgia Extension. Bulletin No. 1245.
Sarmah, A. K., M. T. Meyer, and A. B. A. Boxall. 2006.A global perspective on the use, sales, exposure pathways, occurrence, fate, and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759.
Scott, A., Y. Tien, C. F. Drury, W. Daniel Reynolds, and E. Topp. 2018. Enrichment of antibiotic resistance genes in soil receiving composts derived from swine manure, yard wastes, or food wastes, and evidence for multiyear persistence of swine Clostridium spp. Can. J. Micro. 64:201–208.
Silbergeld, E., M. Davis, B. Feingold, et al. 2010. New infectious diseases and industrial food animal production. Emerg. Infect. Dis. 16:1503–1504.
Sneeringer, S., J. MacDonald, N. Key, W. McBride, and K. Mathews. 2015. Economics of antibiotic use in U.S. livestock production. USDA-ERS Report Number 200. Available at: https://www.ers.usda.gov/webdocs/publications/45485/err-200.pdf?v=2170.2. Accessed: November 5, 2020.
Starr, M. P., and D. M. Reynolds. 1951. Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. Pp 15–34 in: Proceedings of the 51st General Meeting, Society of American Bacteriology, Chicago, IL.
Thanner, S., D. Drissner, and F. Walsh. 2016. Antimicrobial resistance in agriculture. American Society of Microbiology. Available at: https://mbio.asm.org/content/7/2/e02227-15. Accessed: November 9, 2020.
Torsvik, V., L. Øvreås, and T. F. Thingstad. 2002. Prokaryotic diversity: Magnitude, dynamics, and controlling factors. Science 296:1064–1066.
USDA. 2011. Economic Research Service and National Agricultural Statistics Service. 2011 Agricultural and Resource Management Survey (ARMS) broiler survey data.
U.S. Poultry and Egg Association. 2019. Antimicrobial use in poultry. Antimicrobial stewardship within U.S. poultry production 2013–2017 report. Available at: https://www.uspoultry.org/poultry-antimicrobial-use-report/docs/USPOULTRY_Antimicrobial-Report.pdf. Accessed: November 5, 2020.
Vaughn, M. B., and D. Copeland. 2004. Is there human health harm following fluoroquinolone use in poultry? Pages 27–29 in: Proceedings of the 53rd Western Poultry Disease Conference, Sacramento, CA.
World Health Organization. 2011. Tackling antibiotic resistance from a food safety perspective in Europe. Office for Europe Scherfigsvej 8, DK-2100, Copenhagen, Denmark. Available at: https://www.euro.who.int/__data/assets/pdf_file/0005/136454/e94889.pdf?ua=1. Accessed: November 9, 2020.
Yang, Y., A. J. Ashworth, C. Willett, et al. 2019. Review of antibiotic resistance, ecology, dissemination, and mitigation in U.S. broiler poultry systems. Frontiers in Microbiology 10. Article 10. Available at: https://www.frontiersin.org/articles/10.3389/fmicb.2019.02639/full. Accessed: November 9, 2020.
Yang, Y., A. J. Ashworth, J. M. DeBruyn, et al. 2020. Antimicrobial resistant gene prevalence in soils due to animal manure deposition and long-term pasture management. PeerJ. Available at: https://peerj.com/articles/10258/. Accessed: November 10, 2020.
You, Y., and E. K. Silbergeld. 2014. Learning from agriculture: Understanding low-dose antimicrobials as drivers of resistome expansion. Front. Microbiol. 5:284. 10 pages. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4050735/pdf/fmicb-05-00284.pdf. Accessed: November 11, 2020.
Publication 3605 (POD-04-21)
By Tom Tabler, PhD, Extension Professor; Wei Zhai, PhD, Associate Professor; Jessica Wells, PhD, Assistant Clinical/Extension Professor; and Jonathan Moon, Poultry Operation Coordinator, Poultry Science.
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