Paul Ebner
Assistant Professor
Department of
Animal Sciences
Purdue University
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CAFOs and Public Health:
The Fate of Unabsorbed Antibiotics
Note: Traditionally, the term “antibiotic” refers to compounds that are made by microorganisms, usually yeast or bacteria, and kill other microorganisms (e.g., penicillin). Similar compounds that are synthetic or semi-synthetic are more commonly referred to “antibacterials” or “antimicrobials” (e.g., carbadox). Both are used in food animal production, and, for the purpose of this paper, will be grouped simply as “antibiotics.”
Introduction
Antibiotics are used in food animal production in two basic manners: therapeutically (typically higher doses) to treat specific diseases; and subtherapeutically (typically lower doses) for increased feed efficiency or disease prevention. Some antibiotics, however, are not absorbed very well by the animal and are passed in the urine or in manure. As manure is spread on fields as fertilizer, so are the antibiotics. Some see this as a public health concern, believing the drugs could then enter ground or surface water or be taken up by edible plants where the drugs could contribute to antibiotic resistance development and/or adverse reactions in those with antibiotic allergies. What follows is an attempt to address this concern by tracing the life (and activity) of an antibiotic from administration to an animal, to excretion in feces or urine, to application to soil as fertilizer, and finally to possible entry into and contamination of human drinking water or food.
In the Animal
Regardless of the route or purpose of antibiotic use, a portion of the dose will not be absorbed by the animal and will get passed in the urine or feces. The actual amount varies from compound to compound, but in some cases the amount unabsorbed is much greater than the amount absorbed. For example, an estimated 80% of a dose of ampicillin is excreted in urine or feces; in contrast, only 20% of bacitracin is unabsorbed1. Most studies looking at excretion rates report that, in general, the excreted form is the active form of the drug2.
In Manure
In most livestock operations, manure is collected in pits. In some operations, manure is then transferred to lagoons for further remediation. Several studies have detected antibiotics in these environments3,4,5. Whether the drugs remain active in manure pits and lagoons (and for how long) varies from antibiotic to antibiotic. For example, the half-life of tylosin in manure (i.e., the time in which tylosin loses half of its activity) is very short, approximately one week. As such, tylosin is not usually found in high quantities in aged manure. Other drugs, such as 5tetracyclines, are more stable in manure environments and can be detected, albeit at low concentrations, for more than five months5.
In Soil
Manure is usually taken from pits or lagoons and spread on fields both to provide nutrients for crops and to further remediate the manure. It is here that unabsorbed antibiotics are truly introduced to the terrestrial environment. Several groups have shown that varying (usually low) concentrations of active antibiotics can be found in soils treated with livestock manure5,6,7. Once in the soil, the fate of the antibiotic is largely dictated by how well it binds to soil and how quickly it degrades2. Depending primarily on those two factors, the antibiotic can degrade in soil, not degrade and enter surface water as run-off, not degrade and leach into ground water, and/or be taken up by plants.
Regarding degradation, most antibiotics become much less stable once applied to soil, but this too varies from antibiotic to antibiotic. A recent study examining degradation of common veterinary antibiotics in soil reported half-lives of 20, 27, 8, 16, and 5 days for erythromycin, oleandomycin, tylosin, tiamulin, and salinomycin, respectively8. Antibiotics that bind strongly to soil (i.e., are immobilized in soil) and also have shorter half-lives can be completely degraded in soil. Tylosin, for example, binds strongly to soil and has a relatively short half-life. As such, it quickly degrades once applied to soil and is not usually detected in ground water, surface water, or plants.
In Surface Water
Some antibiotics may bind strongly to soil but degrade more slowly. These drugs could enter into surface waterways through run-off. One group reported that 0.091% of sulphachloropyridazine and 0.054% of oxytetracycline applied to a field in manure was lost due to run-off (both aqueous and particulate)9. While these are low amounts, several groups have detected different antibiotics in rivers and streams throughout the United States. In some cases, contamination was attributed to nearby livestock operations10.
In Ground Water
Antibiotics that do not bind strongly to soil are more mobile and have a greater chance of contaminating ground water through leaching. Indeed, several groups have shown that some commonly used antibiotics, namely sulfonamides, can be detected in leachate, albeit at very low levels. It follows that a few studies have reported detecting sulfonamides in well water and one study attributed the contamination to a nearby animal housing facility11. The majority of other antibiotics are not regularly found in leachate.
In Plants
For those antibiotics that bind strongly to soil yet have long half-lives, there is also a concern that these drugs could be taken up by plants. This is only now being researched fully. There are a handful of reports, however, indicating that some plants can take up some antibiotics from soil. This ability apparently varies greatly with both the type of plant and the antibiotic tested. One group showed that corn, green onion, and cabbage absorbed oxytetracycline but not tylosin from spiked soil (i.e., antibiotics added to the soil)12. Another study that more closely resembled real-life conditions (e.g., using actual manure from antibiotic treated animals) showed that of nine antibiotics tested, only three were taken up by lettuce in detectable amounts while four were taken up by carrots. While antibiotics could be detected in the edible portions of the plants, the concentrations at which they were found were much lower than FDA acceptable daily intake levels. The authors concluded that uptake of antibiotics by plants as a result of spreading livestock manure does not pose an appreciable human health risk13.
Significance of These Levels
While there are several studies that assess antibiotic concentrations at single sites such as manure pits, or lagoons, or different soil types, there is a notable lack of integrated studies that trace antibiotic concentrations in several different sites within a single livestock operation. Without such studies, it is difficult to assess the capacity of soil to remove antibiotics from manure.
One such study, however, is available. De Liguoro and co-workers examined antibiotic levels in feces, bedding and manure, soil of fertilized fields, and surrounding drainage courses from a cattle operation following use of both oxytetracycline and tylosin. As was seen in other studies, tylosin degraded very rapidly, was not detected in soil after 45 days, and was never detected in surrounding water. Oxytetracycline was more stable in soil (detectable after five months), but at levels ten times lower than government mandated thresholds. Oxytetracycline was never detected in surrounding water. The authors concluded that spreading manure on soil is effective at eliminating and or destroying unabsorbed antibiotics in manure5.
In place of other integrated investigations, Table 1 is a compilation of several unrelated studies and summarizes the levels at which some antibiotics have been detected in manure, soil, plants, and surface water (compiled from ref. 14). Also included are the FDA acceptable daily intake (ADI) or tolerance levels for each drug. The table suggests that while antibiotic concentrations are initially high in manure samples, there are significant reductions in antibiotic activity with each remediation step. For example, the concentrations detected in soil samples are roughly 1000 fold less than those found in manure. It follows that the levels found in plants or surface water are almost 100,000 fold lower than those found initially in manure and between 20 to 1000 times lower than FDA ADI or tolerance levels.
Finally, it is worth noting that by most accounts the use of antibiotics in food animal production leads to increases in the concentration of antibiotic resistant bacteria in the feces. While the impact this may have on human health is beyond the scope of this current paper, it is important to note that the levels of antibiotics commonly found in waterways or even soil following application of livestock manure are not considered high enough to drive resistance in typical test bacteria (minimum inhibitory concentrations).
Conclusions
Determining the fate of unabsorbed antibiotics in livestock manure is a relatively new field of study. With only a small number of studies, it is difficult to determine whether antibiotics found in livestock manure have an effect on human health once they are released to the terrestrial environment. It is clear that antibiotics can be detected in manure and in soil fertilized with manure. In some cases, antibiotics have been detected in ground or surface water systems near livestock operations. A much smaller number of studies report that some unabsorbed antibiotics can be taken up in small quantities by some plants. A compilation of data from several studies, however, suggests that with each remediation step (e.g., digestion in lagoons, degradation in soil, etc.) the amount of detectable antibiotic drops significantly. As such, the concentrations of antibiotics found in sources that could impact human health such as ground or surface water, or plants, are at least an order of magnitude less than those deemed by the FDA to be an appreciable health risk.
References
(See Lee et al., 2007 and Kumar et al., 2005a for comprehensive reviews)
1. Kummerer K, Henninger A. 2003. Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin Microbiol Infect. 9:1203-1214.
2. Lee LS, Carmosin N, Sassman SA, Dion HM, Sepulveda MS. 2007. Agricultural contributions
of antimicrobials and hormones on soil and water quality. Adv Agron. Vol. 93, Ch. 1. (in press for Jan. 2007)
3. Aga DS, Goldfish R, Kulshrestha P. 2003. Application of ELISA in determining the fate of tetracyclines in land-applied wastes. Analyst. 128:658-662.
4. Kumar K, Thompson A, Singh AK, Chander Y, Gupta SC. 2004. Enzyme-linked immunsorbent assay for ultratrace determination of antibiotics in aqueous samples. J Environ Qual. 33:250-256.
5. De Liguoro M, Cibin V, Capolongo F, Halling-Sorensen B, Montesissa C. 2003. Use of tetracycline and oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere. 52:203-212.
6. Haller MY, Muller SR, McArdell CS, Alder AC, Suter MJF. 2002. Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromotography-mass spectrometry. J Chromot. 952:111-120.
7. Sengelov G, Agerso HSB, Baloda SB, Anderson JS, Jensen LB. 2003. Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int. 28:587-595.
8. Schlusener MP, Bester K. 2006. Persistence of antibiotics such as macrolides tiamulin and salinomycin in soil. Environ Pollut. 143:565-571.
9. Kay P, Blackwell PA, Boxall ABA. 2005. Transport of veterinary antibiotics in overland flow following the application of slurry to arable land. Chemosphere. 59:951-959.
10. Campagnolo ER, Johnson KR, Karpati A, Rubin C, Kolpin DW, Meyer MT, Esteban JE, Currier RW, Smith K, Thu KM, McGeehin M. 2002. Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Sci Total Environ. 299:89-95.
11. Batt AL, Snow DD, Aga DS. 2006. Occurrence of sulfonamide antimicrobials in private water wells in Washington County, Idaho, USA. Chemosphere. 64:1963-1971.
12. Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ. 2005a. Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual. 34:2082-2085.
13. Boxall ABA, Johnson P, Smith EJ, Sinclair CJ, Stutt E, Levy LS. 2006. Uptake of veterinary medicines from soils into plants. J Ag Food Chem. 54:2288-2297.
14. Kumar K, Gupta SC, Chander Y, Singh AK. 2005b. Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron. 87:1-54.
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