Pharm Pollution

Excreted antibiotics can poison plants

by Janet Raloff

Patrick K. Jjemba was curious about the interplay of protozoa and the bacteria they eat in soil. As part of his research, he began altering the organisms' environment. When he applied large amounts of protozoan-killing antibiotics to dirt around the roots of soybeans, Jjemba was amazed at what happened. The drugs widely used in human and veterinary medicine did far more than subtly alter the balance of microbial predators and prey. One drug stunted soybeans, and another killed the plants.

The University of Cincinnati microbiologist realized he was sailing into largely uncharted waters. Though a growing body of research has documented the presence of antibiotics in the environment, most concerns have focused on what harm these antimicrobials might pose to people, fish,or aquatic birds (SN: 3/23/02, p. 182: Available to subscribers at http://www.sciencenews.org/20020323/fob6.asp). These drugs, excreted by people and livestock treated with them, enter open waters primarily from sewage effluent and farm runoff.

The widespread environmental presence of such antibiotics raises the prospect that an increasing share of microbes will become resistant to them (SN: 6/5/99, p. 356: http://www.sciencenews.org/sn_arc99/6_5_99/fob1.htm). However, there's been little discussion of whether these drugs could harm plants.

Farmers apply large quantities of sewage sludge and manure to their fields, yet only a few studies have probed possible crop impacts of the accompanying antibiotics. Preliminary findings from those investigations, most conducted in Europe, paint a disquieting picture: A wide range of plants from weeds to field crops are susceptible to antibiotic poisoning.

Furthermore, plants that aren't severely injured by the drugs might convey antibiotics from the soil into the food supply.

Pooped out

People and livestock collectively shed torrents of urine and mountains of feces into the environment daily. Sewage from some 1 million U.S. households enters the environment essentially untreated (SN: 4/1/00, p. 212: http://www.sciencenews.org/20000401/fob1.asp). Animal wastes sometimes with little processing are applied to farm fields as fertilizer.

Manure and human waste products both can contain residues of drugs. Because the engineers of North America's sewage-treatment plants never designed these facilities to remove excreted drugs, the effluent from such facilities and even some drinking water bears traces of antibiotics and other pharmaceuticals SN: 11/3/01, p. 285: Available to subscribers at http://www.sciencenews.org/20011103/note15.asp). Like manure, leftover solids from sewage treatment plants can carry drug residues, scientists reported in April at an American Water Works Association meeting in Cincinnati.

According to a 1999 report by the Environmental Protection Agency, farmers spread some 7 million tons of sewage sludge known in the trade as biosolids onto fields each year. A recent National Academy of Sciences report indicates that U.S. growers also annually recycle an estimated 3 million tons of manure this way. Not only are biosolids and manure low-cost soil amendments, but their use provides important means of recycling wastes.

The surface water used for irrigation can also host a dozen or more drugs. So, there are plenty of routes by which pharmaceuticals can reach crops. Nobody has yet quantified this contamination.

A quarter-century ago, soil microbiologist Arthur R. Batchelder was disturbed at the thought that people were unwittingly seeding crop soils with antibiotics. Then working for the Agricultural Research Service at Colorado State University in Fort Collins, he focused on farmers who were fertilizing their crops with manure from cattle feedlots. Then, as today, U.S. feedlot operators fed animals antibiotics to promote their growth. Most European countries have banned drug use that's strictly for promoting growth in livestock.

In the early 1980s, Batchelder laced the soil of young greenhouse plants with up to 180 parts per million (ppm) of chlortetracycline or oxytetracycline, which are common livestock-growth promoters. Though radishes, wheat, and corn were unaffected by these antibiotics, pinto bean plants showed ill effects.

Compared with bean plants grown drugfree, those planted in sandy loam soil containing an antibiotic were shorter, weighed less, produced smaller yields of beans, fixed less soil nitrogen, and picked up fewer nutrients from their environment. However, when grown in clay soil, the beans exhibited no effects from the antibiotics. Batchelder speculates that the drugs bound to the clay and remained unavailable to the roots.

In a published report, he concluded that "manure that contains either [antibiotic] should not be applied to sandy loam soil just before pinto beans, and possibly other seed legumes, are planted." Batchelder had hoped to follow up with analyses of the drugs' uptake by plants. "I worried that you might be feeding antibiotics to people," the retired scientist recalls, "but I was pulled off the work."

If Jjemba had been aware of Batchelder's findings, he might have been less startled by the outcome of his studies with soy, another legume. Using chloroquine, quinacrine, or metronidazole, he heavily polluted soil in his lab with drug concentrations between 0.5 and 16 parts per thousand. In the February Chemosphere, he reported that each drug killed the plants, though at different doses.

Working with another antibiotic, sulphadimethoxine, Luciana Migliore of Universita degli Studi "Tor Vergata" in Rome and her colleagues uncovered a similar toxicity in plants other than legumes. In four papers published over the past 6 years, her team showed that the drug can severely stunt the growth of barley, corn, the water fern Azolla filiculoides, and the three common garden weeds redroot pigweed, broad-leafed plantain, and sheep sorrel.

Her group used parts-per-thousand soil concentrations of the drug, which are comparable to those in the manure of swine treated therapeutically, Migliore says.

Root of the problem

Jjemba's studies couldn't establish whether the antibiotics he tested were poisoning plants directly or indirectly by wiping out soil microbes. To resolve that issue, Migliore conducted some of her studies in a sterile, synthetic growth medium. Here, too, antibiotics stunted plant growth.

Overall, Migliore reports that plant development was affected by the type of soil and the concentrations of the drug in the plant. As Batchelder had discovered, the Italian team found that clay tended to bind and disarm the drug. However, Migliore reports that she was surprised to find that all of the plants she assayed took in and stored significant amounts of the drug. Those that took in the most showed the greatest stunting. Among animals on land, pollutants that accumulate in the body tend to be oily compounds preferentially stored in fat. So, many chemists have downplayed the potential for antibiotics, most of which are water-soluble, to accumulate in plants. Migliore now suspects that a plant's reliance on water to deliver its nutrients permits waterborne antibiotics to enter readily. Once inside, the drug can remain in water-rich tissues.

In general, the ecotoxicologist finds that roots accumulate the highest concentrations of drugs. In a 1997 month-long study of barley, she recorded 50 and 80 ppm of an antibiotic in roots, roughly four times the concentration in foliage. Her earlier studies had shown similar patterns in millet, garden peas, and corn.

In an upcoming issue of Water Research, Migliore's team reports that water ferns sop up even more of the drug up to 1,000 ppm in their tissues. Other plants grown in water had lower tissue concentrations but higher values than plants grown in dirt did.

If these antibiotic-storage patterns prove common, crops especially root vegetables and hydroponic crops might carry traces of antibiotics to the dinner table. It's a concern that Migliore plans to address in future experiments.

Stinky science

The researchers' concern would prove moot if antibiotics survived only a few hours in manure or sludge. Recent data, however, suggest that the drugs persist.

For instance, Michael Kühne of the Hannover School of Veterinary Medicine in Germany and his colleagues have studied the longevity of tetracyclines in liquid manure, a slurry of urine and feces. In the United States, feedlot managers frequently administer low doses of tetracyclines to promote the growth of pigs and cattle and higher doses to treat disease. The animals excrete up to 95 percent of a tetracycline administered, Kühne says.

In the July 2000 Journal of Veterinary Medicine A, his group reported that when the liquid manure was kept under conditions resembling those of a typical farm holding tank, concentrations of the antibiotic declined by 50 percent over 8 days. Antibiotic concentrations declined by 70 percent during that period if the sample was ventilated with forced air.

Even this drug-reduction rate "is not really good," Kühne says. "And I would not expect a continuing reduction to zero during storage." What's more, he notes, some of the apparent reduction stems from conversion of the drug to one of its metabolites, which, under certain conditions, can convert back into the parent drug.

Chemist Diana Aga of the State University of New York at Buffalo has made similar observations with liquid manure from swine feedlots in Nebraska. At some stages of the animals' growth, their wastes appear antibiotic-free. Other times, concentrations can run to nearly 1 ppm.

While Aga's preliminary data indicate that the drugs begin breaking down under exposure to sunlight with reductions of perhaps 50 percent in a week she notes that at least in Nebraska, livestock producers typically truck their manure offsite quickly. In some cases, she says, "it could be on fields within several days."

Large, fuzzy estimates

With large parcels of cropland relying on such natural fertilizers, wouldn't crop losses already have been reported if antibiotics injure plants? They might be difficult to detect. Soil scientist Chi Chang of Agriculture and Agri-Food Canada's research center in Lethbridge, Alberta, notes that the chemical makeup of manure can vary even between batches, depending on what the animals have been fed, their health, and how wastes have been handled. Moreover, a drug's role in the health and yields of crops might be camouflaged by effects of weather, rainfall, and pests.

In fact, Migliore doubts that antibiotic tainting of manure and sludge is high enough today to cause anything beyond subtle crop-yield declines that could easily be attributed to something else.

But that could change, she and others worry. If some antibiotics prove persistent in the environment, they could gradually accumulate in soils. Moreover, if drug-use or fertilization rates increase on farms, crop effects might also.

Right now, projecting antibiotic trends is hampered because "in North America, there's no systematic collection of antibiotics-use data, either in human or veterinary medicine," notes veterinary epidemiologist Scott McEwan of the University of Guelph in Ontario. The estimates, he notes, are "all over the map."

In a May report by the Boston-based Alliance for the Prudent Use of Antibiotics, McEwan and Paula J. Fedorka-Cray of the U.S. Agricultural Research Service in Athens, Ga., highlight those inconsistencies.

Two-year-old figures from the pharmaceutical industry estimate that 14.7 million pounds of veterinary antibiotics go to treat disease annually and another 3.1 million pounds are used as growth-promoting feed additives.

Last year, the Boston-based Union of Concerned Scientists offered numbers that contradict the alliance's: just 2 million pounds for veterinary therapy and an estimated 27.5 million pounds for growth promotion. The group noted that people consume only 4.5 million pounds of antibiotics annually.

Whatever the number for total antibiotic usage, it's huge. That's why Aga's team has begun investigating factors such as sunlight, composting, and ventilation that farmers might employ to help break down the antibiotics in fertilizers made from wastes. After all, she says, "we recognize the importance of fertilizing fields with manure and sludge."

References: Batchelder, A.R. 1982. Chlortetracycline and oxytetracycline effects on plant growth and development in soil systems. Journal of Environmental Quality 11(October):675-678.

Batchelder, A.R. 1981. Chlortetracycline and oxytetracycline effects on plant growth and development in liquid cultures. Journal of Environmental Quality 10(October):515-518.

Chang, C., T.G. Sommerfeldt, and T. Entz. 1993. Barley performance under heavy applications of cattle feedlot manure. Agronomy Journal 85:1013-1018.

Forni, C., et al. In press. Sulphadimethoxine and Azolla filiculoides lam.: A model for drug remediation. Water Research.

Jjemba, P.K. In press. The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: A review. Agriculture, Ecosystems and Environment.

Jjemba, P.K. 2002. The effect of chloroquine, quinacrine, and metronidazole on both soybean plants and soil microbiota. Chemosphere 46(Feb.):1019-1025.

Kühne, M., et al. 2000. Stability of tetracycline in water and liquid manure. Journal of Veterinary Medicine A 47(July):379-384.

McEwen, S.A., and P.J. Fedorka-Clay. 2002. Antimicrobial use and resistance in animals. Clinical Infectious Diseases 34(June 1):S93-S106.

Migliore, L., et al. 1997. Toxicity of several important agricultural antibiotics to Artemia. Water Research 31:1801-1806.

Migliore, L., et al. 1997. Effects of sulphadimethoxine on cosmopolitan weeds (Amaranthis retroflexus L., Plantago major L. and Rumex acetosella L.). Agriculture, Ecosystems and Environment 65:163-168.