The drugs fed to farm animals and the risks posed to humans

REUTERS/Max Whittaker

Documents reveal how poultry firms systematically feed antibiotics to flocks

FIGHTING SALMONELLA: Foster Farms chief veterinarian Bob O’Connor checks a flock of chicks at the company’s Fox Ranch complex in Stanislaus County, California, in June. Two months earlier, the company scrubbed the barn clean after discovering Salmonella Heidelberg, a pathogen which U.S. authorities linked to Foster Farms chicken and blamed for sickening more than 600 people. REUTERS/Max Whittaker

Part 1: Pervasive use fuels concerns about impact on human health, emergence of resistant superbugs

Major U.S. poultry firms are administering antibiotics to their flocks far more pervasively than regulators realize, posing a potential risk to human health.

Internal records examined by Reuters reveal that some of the nation’s largest poultry producers routinely feed chickens an array of antibiotics – not just when sickness strikes, but as a standard practice over most of the birds’ lives.

In every instance of antibiotic use identified by Reuters, the doses were at the low levels that scientists say are especially conducive to the growth of so-called superbugs, bacteria that gain resistance to conventional medicines used to treat people. Some of the antibiotics belong to categories considered medically important to humans.

The internal documents contain details on how five major companies  - Tyson Foods, Pilgrim’s Pride, Perdue Farms, George’s and Koch Foods - medicate some of their flocks.

The documented evidence of routine use of antibiotics for long durations was “astonishing,” said Donald Kennedy, a former U.S. Food and Drug Administration commissioner.

Kennedy, president emeritus of Stanford University, said such widespread use of the drugs for extended periods can create a “systematic source of antibiotic resistance” in bacteria, the risks of which are not fully understood. “This could be an even larger piece of the antibiotic-resistance problem than I had thought,” Kennedy said.

Reuters reviewed more than 320 documents generated by six major poultry companies during the past two years. Called “feed tickets,” the documents are issued to chicken growers by the mills that make feed to poultry companies’ specifications. They list the names and grams per ton of each “active drug ingredient” in a batch of feed. They disclose the FDA-approved purpose of each medication. And they specify which stage in a chicken’s roughly six-week life the feed is meant for.

The feed tickets examined represent a fraction of the tens of thousands issued annually to poultry farms run by or for major producers. The confidential information they contain nonetheless extends well beyond what the U.S. government knows. Veterinary use of antibiotics is legal and has been rising for decades. But U.S. regulators don’t monitor how the drugs are administered on the farm – in what doses, for what purposes, or for how long. Made public here for the first time, the feed documents thus provide unique insight into how some major players use antibiotics.

The tickets indicate that two of the poultry producers - George’s and Koch Foods - have administered drugs belonging to the same classes of antibiotics used to treat infections in humans. The practice is legal. But many medical scientists deem it particularly dangerous, because it runs the risk of promoting superbugs that can defeat the life-saving human antibiotics.

In interviews, another major producer, Foster Poultry Farms, acknowledged that it too has used drugs that are in the same classes as antibiotics considered medically important to humans by the FDA.

About 10 percent of the feed tickets reviewed by Reuters list antibiotics belonging to medically important drug classes. But in recent presentations, scientists with the U.S. Centers for Disease Control and Prevention said the use of any type of antibiotic, not just medically important ones, contributes to resistance. They said that whenever an antibiotic is administered, it kills weaker bacteria and enables the strongest to survive and multiply.

Frequent, sub-therapeutic use of antibiotics in low doses intensifies that effect, scientists and public health experts say. The risk: Any resulting superbugs might also develop cross-resistance to medically important antibiotics.

According to the feed tickets reviewed, low doses of antibiotics were part of the standard diet for some flocks at five companies: Tyson, Pilgrim’s, Perdue, George’s and Koch.

“These are not targeted uses aimed at specific bugs for defined duration. They’re multiple, repeat shotgun blasts that will certainly kill off weaker bugs and promote the stronger, more resistant ones," said Keeve Nachman, director of the food production and public health program at Johns Hopkins University’s Bloomberg School of Public Health.


This month, Perdue Farms announced that it had stopped applying the antibiotic gentamicin to eggs in chicken hatcheries. Gentamicin is a member of an antibiotic class considered “highly important” in human medicine by the FDA. The company said it wants “to move away from conventional antibiotic use” because of “growing consumer concern and our own questions about the practice.”

The move won’t change what Perdue feeds its chickens, however. Some of its feed has contained low levels of one antibiotic, feed tickets show. Perdue said it only uses antibiotics that aren’t considered medically important by the FDA, and at some farms, it uses no antibiotics at all.

MEDICATED FEED: Nine-day-old chicks drink water at a Foster Farms ranch in Stanislaus County, California. Chicks are typically given various pharmaceuticals, including vaccines and low-level doses of antibiotics, in their water or food to ward off disease. REUTERS/Max Whittaker

The manner in which drugs are being given to poultry shows that “this could be an even larger piece of the antibiotic-resistance problem than I had thought.”

Donald Kennedy, former FDA commissioner

“We recognized that the public was concerned about the potential impact of the use of these drugs on their ability to effectively treat humans,” Bruce Stewart-Brown, Perdue’s senior vice president of food safety and quality, said when the hatchery policy was announced.

The poultry industry’s lobby takes issue with the concerns of government and academic scientists, saying there is little evidence that bacteria which do become resistant also infect people.  

"Several scientific, peer reviewed risk assessments demonstrate that resistance emerging in animals and transferring to humans does not happen in measurable amounts, if at all," said Tom Super, spokesman for the National Chicken Council. He said using antibiotics to prevent diseases in flocks “is good, prudent veterinary medicine…. Prevention of the disease prevents unnecessary suffering and prevents the overuse of potentially medically important antibiotics in treatment of sick birds.”

Poultry producers began using antibiotics in the 1940s, not long after scientists discovered that penicillin, streptomycin and chlortetracycline helped control outbreaks of disease in chickens. The drugs offered an added benefit: They kept the birds’ digestive tracts healthy, and chickens were able to gain more weight without eating more food.

Over the years, the industry’s use of antibiotics grew. Early on, independent scientists warned that bacteria would inevitably develop resistance to those antibiotics, especially when the drugs were administered in low doses. In 1976, a landmark study by microbiologist Stuart Levy showed that potentially deadly bacteria in poultry were developing resistance to tetracyclines and other antibiotics. The resistant bacteria, E. Coli, were then moving from poultry to people.

That is when the FDA first tried to rein in drug use in food animals. The agricultural and pharmaceutical industries resisted, viewing low-level antibiotic use as a way to produce meat more quickly and cheaply.

Today, 80 percent of all antibiotics used in America are given not to people, but to livestock.

About 390 medications containing antibiotics have been approved to treat illness, stave off disease and promote growth in farm animals. But the FDA has reviewed just 7 percent of those drugs for their likelihood of creating antibiotic-resistant superbugs, a Reuters data analysis found.

The widespread use of antibiotics worries public health authorities. In a report this year, the World Health Organization called antibiotic resistance “a problem so serious it threatens the achievements of modern medicine.” The annual cost to battle antibiotic-resistant infections is estimated at $21 billion to $34 billion in the United States alone, the WHO said.

Each year, about 430,000 people in the United States become ill from food-borne bacteria that resist conventional antibiotics, according to a July report by the CDC. Overall, the CDC estimates that 2 million people are sickened in the United States annually with infections resistant to antibiotics. At least 23,000 people die.

“That’s the number we are certain of. The actual number is higher,” said Steve Solomon, director of the CDC’s Office of Antimicrobial Resistance.

This year, federal investigators tracking a salmonella outbreak traced virulent strains of the pathogen to chickens raised by Foster Farms, the largest poultry producer on the West Coast.

Investigators identified seven strains of Salmonella Heidelberg that had sickened at least 634 people across the United States and Puerto Rico this year and last. More than 200 of those people were hospitalized, according to the CDC. In July, Foster Farms issued a recall of some chicken products.

When epidemiologists examined 68 of the Salmonella Heidelberg cases linked to Foster Farms, they found that two-thirds of the bacteria were resistant to at least one antibiotic, according to the CDC. Half of these superbugs were impervious to drugs in at least three different classes of antibiotics.

In an effort to stop the spread of resistant bacteria, the FDA has issued voluntary guidelines to regulate antibiotic use by producers of poultry and other livestock. The agency says it also inspects the mills where animal feed is made. It considers those inspections to be a “more effective” use of its resources than examining how farmers administer feed.

“These are not targeted uses aimed at specific bugs for defined duration. They’re multiple, repeat shotgun blasts that will certainly kill off weaker bugs and promote the stronger, more resistant ones.”  

Keeve Nachman, Johns Hopkins University

Not until 2016 does the FDA plan to gather data about antibiotic use on farms, said Craig Lewis, a veterinary medical officer with the agency. Today, “none of us have an idea first-hand of what’s going on” at the farm level, Lewis said this summer, at a public meeting on antibiotic resistance.

Super, the National Chicken Council spokesman, said the information on feed tickets “is available to FDA, the regulators, whenever they want to go see it.”

Still, companies are reluctant to discuss how they medicate their flocks.

One, Pilgrim’s Pride, said it would take legal action against Reuters unless the news agency gave the company access to Pilgrim’s feed tickets that reporters had reviewed. Reuters declined to do so.

The tickets show that Pilgrim’s added low doses of the antibiotics bacitracin and monensin, individually or in combination, to every ration fed to a flock grown early this year. Neither drug is classified as medically important by the FDA, although bacitracin commonly is used to prevent human skin infections.

The Colorado-based company wouldn’t address questions about its use of antibiotics. Its general counsel, Nicholas White, called the contents of its tickets “confidential business information.”

U.S. Sen. Kirsten Gillibrand, D-New York, said the feed tickets substantiate what she long suspected: "that the overuse of antibiotics on many chicken farms is rampant.”

Gillibrand has been pushing for regulators to more aggressively monitor low-level doses of antibiotics. Now, Gillibrand said, she hopes “the FDA will use the feed-ticket data obtained by Reuters as a wake-up call to re-evaluate their approach to the regulation of antibiotic use in food production.”

So does Rep. Rosa DeLauro, D-Connecticut, a member of a House subcommittee overseeing food safety. Told of the information in the feed tickets, DeLauro called on the FDA to “implement tighter restrictions on antibiotic usage.”


All the poultry giants state publicly that they use antibiotics for the limited purpose of keeping chickens healthy.

But the feed tickets, which list the medications included in chicken feed, highlight a second effect of many of the drugs: bulking up the birds.

Some of the tickets reviewed for this article state that the antibiotics promote feed efficiency or weight gain in chickens. The FDA requires companies to list growth promotion on feed tickets whenever feed includes antibiotics that have been approved for that purpose.

Reuters found eight different antibiotics listed on the tickets it reviewed. The tickets come from a scattering of farms across the United States – in Mississippi, Alabama, South Carolina, Virginia and Washington State, among other locations.

George’s Inc, a poultry company based in Springdale, Arkansas, issued feed tickets last year to a chicken grower in Virginia. The tickets show that the antibiotics tylosin and virginiamycin were administered solely for “increased rate of weight gain.”

Tylosin belongs to a class of antibiotics the FDA considers “critically important” in human medicine, the most crucial of three ranks of sensitive drugs. Virginiamycin is part of a class in the FDA’s middle rank, “highly important.”

Other George’s Inc feed tickets, given to two growers in Virginia this year, show the antibiotics bacitracin and narasin and a non-antibiotic drug called nicarbazin were included in every poultry ration in different combinations until shortly before slaughter. Bacitracin can promote growth.

George’s said in a statement: “Occasionally (when necessary to control certain pathogens) appropriate FDA approved medications are utilized to prevent, control or treat specific diseases.” It declined to answer detailed questions.

Use of antibiotics to stave off disease in flocks “is good, prudent veterinary medicine…. Prevention of the disease … prevents the overuse of potentially medically important antibiotics in treatment of sick birds.”

Tom Super, National Chicken Council

At Tyson Foods, two feed tickets sent by the company to two Mississippi farms show that bacitracin and the non-antibiotic nicarbazin were among the drugs mixed into the feed. The tickets state the drug combination is “for use in the prevention of coccidiosis in broiler flocks, growth promotion and feed efficiency.” Coccidiosis is a common intestinal ailment.

Tyson, also based in Springdale, Arkansas, said it does not use bacitracin to promote growth, only to prevent disease. The FDA requires companies to list growth promotion on tickets if medications have that effect, Tyson said. The company said that its feed mixture changes throughout the year. In some seasons, it said, the feed doesn’t include bacitracin and nicarbazin.

At Koch Foods Inc, a Chicago-based supplier to fast-food chain KFC Corp, feed tickets contradict a statement on the Koch website about antibiotic use.

Until Aug. 27, the website said Koch Foods uses antibiotics for the narrow purpose of protecting the health of its chickens. “We do not administer antibiotics at growth promotion doses,” the statement read in part. “No antibiotics of human significance are used to treat our birds.”

Koch feed tickets dated from Nov. 30, 2011, through July 20, 2014, indicate otherwise. They list low-dose amounts of five different types of antibiotics in feed given to flocks at one Alabama farm. One was virginiamycin, in a class considered “highly important” to fighting infections in humans.

In 34 of the 55 Koch Foods feed tickets that Reuters examined, antibiotics at low-dose levels were listed “for increased rate of weight gain,” a related growth-promotion use called “improved feed efficiency,” or both. Each of those feed tickets also said the antibiotics were for the prevention of coccidiosis, another bacterial infection, or both.

Koch Foods changed the website after being asked by Reuters about its use of virginiamycin. “I regret the wording mistake on that particular letter” on the website, said Mark Kaminsky, Koch’s chief financial officer. The company said it is required by the FDA to list certain drugs as growth promoters if they have that effect; Koch says it does not use them for that purpose.

Koch said it has no plans to discontinue the use of virginiamycin, which it says may be used to prevent a common intestinal infection in chicken.

KFC U.S. said in a statement: “KFC’s supply partners must adhere to our strict standards and specifications, which in some cases are more stringent than the FDA’s regulations.” A spokeswoman didn’t address detailed questions about antibiotic use by Koch Foods and KFC’s other chicken suppliers.


The experience of one grower raises questions about whether preventive use of antibiotics has a meaningful effect on the health of chicken.

Craig Watts, who grows chicken for Perdue, says he sees little difference in outcomes for the birds he raises on feed containing an antibiotic and those he grows for the company’s antibiotic-free line.

Perdue mixes the antibiotic narasin into feed given to chickens in the company’s antibiotic-fed line. Its antibiotic-free line contains antimicrobial drugs that kill micro-organisms, but none that the FDA defines as an antibiotic, according to Perdue feed tickets shown by Watts. None of the drugs listed by Perdue on the feed tickets is considered medically important for humans.

Watts owns C&A Farms, about 20 miles north of Dillon, South Carolina. Since 2012, he has raised five antibiotic-free flocks for Perdue and seven flocks that received low doses of the antibiotic narasin, according to his records.

SAFETY CHECK: Craig Watts, a contract farmer for Perdue Farms, checks a euthanized chicken for disease. He says he finds little difference in outcome between chickens that are fed antibiotics and those that aren’t. REUTERS/Randall Hill

The mortality rates of the two flock types were nearly identical. About 900 birds died, per house, on the four-house farm. Flocks that received antibiotics and those that didn’t both hit Perdue's target weight of about 4.25 pounds per bird.

Perdue sees “similar” performance among birds fed antibiotics and those that do not receive the drugs, said Stewart-Brown, the Perdue official overseeing food safety. “We feel our current two approaches are both very responsive to public health concerns about antibiotic use in poultry.”

Perdue still uses antibiotics in some cases, because antibiotic-free flocks are “more expensive to run and more difficult to manage effectively,” Stewart-Brown said. The production complex served by Watts’ farm recently transitioned to all antibiotic-free flocks.


One poultry giant whose antibiotic use has come into question is Foster Farms, based in Livingston, California. Its experience shows the difficulty of pinpointing when and how a bacteria turns into a superbug, say federal investigators.

Beginning last year, a salmonella outbreak spread across Oregon, Washington, California and 27 other states and territories. Federal investigators later linked the outbreak to chickens raised by Foster Farms and processed at a trio of its slaughterhouses in central California, according to USDA and CDC officials.

The scope of the outbreak reflected Foster Farms’ vast scale. Its operations in California’s Central Valley date to 1939, when Max and Verda Foster borrowed $1,000 against a life insurance policy and invested in an 80-acre farm.

Today, Foster owns large tracts of California farmland, chicken hatcheries in Colorado and train cars that haul grain from the Midwest. An estimated one of 10 chickens eaten in the United States is hatched, raised and slaughtered by Foster Farms, according to industry officials. The company dominates the chicken market west of the Rocky Mountains.

As the CDC studied what investigators informally called the “Foster Farms Outbreak,” researchers soon made a troubling discovery. Some of the Salmonella Heidelberg strains linked to Foster products proved resistant to a variety of antibiotics, the CDC concluded. Some of those drugs belonged to the same classes as penicillin and chlortetracycline, or CTC.

“The overuse of antibiotics on many chicken farms is rampant.”

U.S. Sen. Kirsten Gillibrand, D-New York

Some questions remain. Government investigators didn’t determine how the Salmonella Heidelberg traced to Foster Farms became resistant to antibiotics, and didn’t trace the resistant bacteria to specific farms. They didn’t examine Foster feed tickets from the outbreak period to see which antibiotics the company was using and how the drugs were being administered.

Reuters asked to see Foster Farms’ feed tickets from that period; the company didn’t respond to that request.

Foster Farms said it commissioned research that yielded findings very different from the CDC’s. The company declined to share the study. It summarized the research by saying scientists found no antibiotic resistance in two dozen salmonella samples collected from Foster Farms in 2012.

A CDC spokeswoman said the agency is aware that Foster Farms sponsored a study and has asked to review it, but hasn’t received a copy.

Foster Farms told Reuters it has administered CTC and penicillin at times, but selectively, not as part of standard feed. Foster said it had used CTC “as needed” to fight bacterial infections. It declined to say where or when it administered CTC. The company said it still uses penicillin to treat sick birds, but only “in critical situations when flocks are exposed to fatal diseases.” Foster doesn’t use antibiotics as growth promoters, it said.

CDC official Robert Tauxe helped investigate the outbreak. “Use of chlortetracycline could have contributed to the resistance patterns we saw” in the Salmonella Heidelberg, said Tauxe. “Penicillin, too.”

On July 11, the CDC said the Salmonella Heidelberg outbreak had ended. The USDA said it is monitoring the company’s new salmonella-prevention efforts. Agency officials and Foster’s chief veterinarian, Bob O’Connor, said the measures are working.

The company has reduced salmonella-infection rates on chicken meat from its California facilities to less than 3 percent, O’Connor said, far below the national average of 25 percent.

Despite the gains, O’Connor said the challenge of eradicating salmonella in the chicken industry remains. “For the people who wanted a silver-bullet-type story, there isn't one,” O’Connor said. “With salmonella, we're not going to be able to say, ‘It's over.’”

David Acheson, a former senior medical officer for the USDA and the FDA, now serves on a food safety advisory board for Foster Farms. He said the board never examined Foster’s use of antibiotics and whether its practices could have spawned superbugs.

“Does anyone know that it happened? No. Is it possible? Could it have happened? Yes,” Acheson said. “We know that antibiotic use, irrelevant of what you are treating, whether it be human or animal, can increase the likelihood of resistance. It’s biology at work.”

Reporting by P.J. Huffstutter in Chicago and Livingston, California, Brian Grow in Atlanta and Fairmont, North Carolina and Michael Erman in New York. Additional reporting Eric Johnson. Edited by David Greising and Blake Morrison.

On American dairy farms, sharp rise in the misuse of a potent but risky drug

ESSENTIAL INGREDIENTS: Hugh Byron, a retired dairy farmer, shows a syringe he used to treat cows at his farm in Hillsboro, Kentucky. Regulators found that one of his cows tested positive for 14 times the allowable trace levels of ceftiofur, an antibiotic that has been found to promote superbugs. REUTERS/John Sommers II

Part 2: The antibiotic ceftiofur is a wonder drug for dairy farmers. But its strength - and the frequency at which it’s used improperly in cattle - pose a threat to public health.

NEW YORK/ATLANTA – It is one of the most potent antibiotics used by U.S. cattle and dairy farmers, the key component in the top-selling drug line of Zoetis, the world’s largest animal health company.

But the strength of the antibiotic ceftiofur – and the frequency with which it’s being misused on farms across America – has created a threat to human health that may overshadow the drug’s effectiveness, a Reuters examination shows.

The U.S. Food and Drug Administration cautioned in 2012 that ceftiofur could pose a “high public health risk,” in part because the drug belongs to a class of antibiotics considered critically important in human medicine. The warning is the FDA’s strongest kind. The concern is that ceftiofur in animals could spawn antibiotic-resistant bacteria, superbugs that can infect people and defeat conventional medical treatment, even when the drug is used as directed.

A Reuters analysis of government data indicates that the risks to human health may be more significant than previously known. Since last year, records kept by the U.S. Department of Agriculture show that traces of ceftiofur were found at illegal levels in slaughtered animals more frequently than with any other drug. In 2013, ceftiofur alone accounted for one-fourth of all residue violations logged by the USDA, the data show.

The ceftiofur residues are not themselves considered dangerous to people if ingested, because the government sets its standards well below hazardous levels.

But the traces serve as a warning sign that the drug was used shortly before the animal was killed, thus increasing the chances that the meat contains superbugs, said Guy Loneragan, a veterinary epidemiologist at Texas Tech University. Studies show that ceftiofur, more than most other drugs, can sharply increase the amount of antibiotic-resistant bacteria in an animal.

“It kills off weaker bugs and allows stronger ones to survive and multiply,” Loneragan said. The effect is especially pronounced soon after the drug has been used, studies show.

Zoetis says ceftiofur is safe to use as directed.  “The use of ceftiofur continues to be appropriate when used according to the label directions in those animals that are in at-risk situations,” said Scott Brown, vice president of global therapeutics research at Zoetis.

The stakes are especially high because the drug is part of a crucial class of antibiotics called cephalosporins. The class includes ceftriaxone, a drug that’s vital to treating pneumonia, meningitis and salmonella infections in children, according to the FDA. The use of one type of cephalosporin can compromise the effectiveness of others in the same class.

“There is a very clear link between ceftiofur use and ceftriaxone resistance,” said Paul Fey, a professor of microbiology at University of Nebraska Medical Center. “We know that ceftiofur-resistant salmonella are clearly ceftriaxone-resistant.”

Despite the perils, there are economic incentives to misuse ceftiofur. The potent drug can keep a sick cow alive long enough for a dairy farmer to sell the animal to a slaughterhouse. A course of treatment can cost from $20 to more than $100, relatively high for veterinary antibiotics. But that is far less than what the farmer stands to make if the animal survives until it can be sold for meat. Dairy cows for slaughter are now fetching $1,500 or more, according to farmers and USDA data.

Hugh Byron ran a dairy farm in Hillsboro, Kentucky, until 2011 and kept cattle until this year. He says he frequently used ceftiofur to treat common infections in his cows. In July 2010, a dairy cow sent to slaughter from Byron’s farm tested positive for 5.61 milligrams of ceftiofur residue per kilogram of tissue sample. That was 14 times higher than the 0.4 milligram per kilogram tolerance level set by the FDA.

COSTS AND BENEFITS: Byron at his 175-acre farm. Ceftiofur is a money-saver for dairy farmers, a point featured by manufacturer Zoetis in its marketing. Short withdrawal times for the drug mean farmers can keep cows milking while they are sick. Ceftiofur can also keep a sick cow alive long enough for a farmer to sell it off to a slaughterhouse. REUTERS/John Sommers II

“We’re talking about our livelihood, our money.... So there’s a temptation to fudge on it.”

Hugh Byron, retired dairy farmer

Byron admits that he has administered ceftiofur at the end of his animals’ lives hoping they’d hang on, so that a slaughterhouse would accept the cows and pay him.

“We’re talking about our livelihood, our money. We’re trying to save the cow and if we can’t save the cow, we’re trying to salvage it,” said Byron. “In other words, send her to the stockyard and get something out of it. So there’s a temptation to fudge on it.”

Zoetis features the drug’s economic advantages in its marketing to farmers and veterinarians. One of ceftiofur’s features is a short withdrawal period - the FDA-mandated time between when an animal stops taking an antibiotic and when its milk or meat is certain to be sufficiently free of residue to pass inspection.

The drug’s time advantage is significant. In the case of milk, if a cow takes penicillin, the farmer must discard all the milk produced for at least two days and as many as 15 days after the drug is last given. There’s often no withdrawal period for certain ceftiofur products, so a cow can keep producing milk while taking it.  

“No wasted milk ensures a better return on investment,” Zoetis says on its website about its ceftiofur-brand drug Excenel.

The residue-testing program is supposed to help the government ensure that farmers are not misusing the drugs.  The regulations contain a gap, however. The USDA tests animals for traces of antibiotics, to prevent excess levels of drugs such as ceftiofur from entering the food supply. But the residue program doesn't test for the presence of resistant bacteria. In the case of ceftiofur, those bugs can survive in an animal past the end of the drug's required withdrawal period, studies show.

Loneragan of Texas Tech said his research suggests the FDA should analyze whether high levels of resistant bacteria remain beyond the withdrawal period. A longer period may be warranted, he said, to ensure that the resistant bacteria population is reduced before the animal is slaughtered.

The reason for the rise in ceftiofur violations isn’t clear. The USDA implemented a new test in 2012 that it says is better at identifying traces of all drugs. But the USDA residue data don’t show as large an increase in violations for penicillin and other antibiotics as they do for ceftiofur.

FDA spokeswoman Juli Putnam said the agency “is aware of the increase in ceftiofur residue violations” and is gathering more information to “better understand the matter.” She said the agency is aware of Loneragan’s research findings as well, “and we continue to consider the evolving science related to the impact of antimicrobial use on bacterial populations.”

Zoetis said the FDA has evaluated ceftiofur’s impact on antibiotic resistance in bacteria and has approved drugs containing the compound as recently as last year.

Those caught misusing veterinary antibiotics face light consequences. Penalties include condemnation of the animal. FDA inspectors review a violator’s practices, which can result in warning letters ordering farmers to change how they administer the medicines. Further action is extremely rare, an examination of regulatory and court records shows.

The residue testing program has been harshly criticized by federal auditors. A 2010 report by the Government Accountability Office found that the program "is not accomplishing its mission of monitoring the food supply for harmful residues." One result of the audit was the implementation two years later of the new residue testing methodology now used by the USDA and FDA.  

SUCCESSFUL DRUG                                  

The widespread application of antibiotics in veterinary medicine poses enormous challenges for health authorities. Today, 80 percent of all antibiotics used in the United States are given to livestock, not to people. In September, Reuters documented how some of America’s largest poultry companies routinely mix low levels of antibiotics into the feed given to chickens, a practice that scientists believe is especially conducive to the growth of superbugs.

About 2 million people in the United States are sickened each year by bacterial infections that resist conventional antibiotics, and at least 23,000 people die, according to the U.S. Centers for Disease Control and Prevention. The World Health Organization called antibiotic resistance “a problem so serious it threatens the achievements of modern medicine.”

Despite such concerns, sales of antibiotics for use in food animal production rose 16 percent by volume from 2009 to 2012, government data show. Sales of cephalosporins increased at more than twice that rate.

The government has made some effort to curb ceftiofur use because of concerns about antibiotic resistance. The FDA requires farmers to obtain a prescription from a veterinarian. In 2012, the agency issued an order prohibiting most off-label uses of the drug, pointing to residues as one contributing factor.

The rise in ceftiofur use is a boon to its largest maker, Florham, NJ-based Zoetis, the former animal drug unit of pharmaceutical giant Pfizer Inc. Ceftiofur-based brands are the company’s top-selling line, generating about $300 million in revenue per year since 2011, according to company financial reports.

Zoetis markets its ceftiofur brands to veterinarians, who must prescribe the drug, and to farmers in YouTube videos and in veterinary and dairy publications. The drug has become one of the most popular antibiotics on American cattle farms. Veterinarians and farmers praise its potency, efficiency and ability to treat multiple ailments, from foot rot to bovine respiratory disease.

MODERN METHODS: Cattle grazing in Hillsboro, Kentucky. Eighty percent of all antibiotics used in the United States are given to livestock, not people. The government tests fewer than 1 percent of cattle for antibiotic residue. REUTERS/John Sommers II

“We had to use so little of it for such a huge effect,” said H. Morgan Scott, a veterinary epidemiologist at Texas A&M University’s College of Veterinary Medicine.

Another selling point is the drug’s short withdrawal times. FDA withdrawal guidelines are based on the presence of antibiotic residue in meat. Compared with other antibiotics, ceftiofur is metabolized rapidly by cows – and so regulators require a shorter waiting period. The drug’s withdrawal periods are zero to three days for milk and four to 13 days for meat. With other drugs, the ranges can be four weeks or more for meat.

Those short windows leave a potential safety gap. Even when ceftiofur is used as approved, one 2007 study shows, antibiotic-resistant bacteria remained present in the guts of cattle long after the drug was given. The FDA cited the study, whose authors include Loneragan and Scott, in the 2012 order reining in use of the drug.

The study, published in the American Journal of Veterinary Research, found that one properly administered dose of a ceftiofur-based medication made by Zoetis resulted in 40 percent of the surviving E. coli in cattle having resistance to ceftiofur six days after the dose. The resistant bacteria population remained above 20 percent of the total for two weeks. Resistant bacteria did not return to levels typical in untreated cattle for 28 days, well after ceftiofur’s withdrawal period, the study found.

As part of the USDA’s National Residue Program, food safety regulators test meat for drugs and chemicals that could prove dangerous to consumers. In 2012, the USDA tested for drug residues in about 185,000 cattle – far less than 1 percent of the more than 33 million cattle slaughtered in the United States that year. The percentage of pigs, poultry and other animals tested is lower.

If high drug residues are found, the results are turned over to the FDA for investigation and enforcement.

In 2013, no single drug residue was found more frequently in slaughtered animals than ceftiofur, the Reuters analysis shows.

Violations involving high levels of ceftiofur in meat rose by 323 percent between 2008 and 2013 – from 98 violations to 415. Last year alone, more than a quarter of all 1,634 residue violations were for ceftiofur – more than four times its share of violations in 2008, the analysis shows. Violations involving ceftiofur have continued at a similar rate during the first half of 2014.

BUSINESS BASICS: Hugh Byron shows some of the medicine he once used to treat his herd. REUTERS/John Sommers II

“These are animals that probably should not have gone to slaughter.”

John Hallberg, director of U.S. regulatory affairs at Zoetis

Dairy cows are one of America's major sources of ground beef, which in turn is the beef product most prone to bacterial infections. Dairy cows are also the leading source of ceftiofur residues, representing 76 percent of the 415 violations in 2013. Last year, 45 percent of the 1,634 residue violations for all drugs were found in dairy cows.

Zoetis said it was aware of the residue violations but that they were small in number, and most – perhaps all – of the animals were pulled from the food supply when residues were found.

“These are animals that probably should not have gone to slaughter, or there were mistakes and animals go to slaughter that didn’t follow withdrawal periods,” said John Hallberg, director of U.S. regulatory affairs at Zoetis.


Ceftiofur can save farmers money by keeping a cow milking longer and by preserving her value at the slaughter stage. In its marketing materials, Zoetis zeroes in on some of the savings.

In one pitch, it says that using its Excede brand instead of penicillin to treat dairy cows with bovine respiratory disease could save a farmer more than $30 per animal, after factoring in the value of milk production not lost to withdrawal.

The company makes a similar case for Excenel. “Protect your cows and your bottom line with EXCENEL,” its website says.

There are also gains to be had at life’s end. Because of the short withdrawal times, farmers can get paid more quickly after treating the animal.

“Shorter meat withdrawals. You’d have to wait 29 days longer” when using a rival drug, says an advertisement for Excede.

Time is money for a farmer with a gravely ill cow on his hands. Interviews with farmers, veterinarians and field researchers, and a review of FDA warning letters, show ceftiofur has been administered to animals by farmers eager to keep a sick animal alive long enough to sell it.

Byron, the 66-year-old retired dairyman in Kentucky, says ceftiofur is a wonder drug. It’s one of the more effective antibiotics, he found, and treated animals and their milk don’t have to be kept off market for long.

“Our attitude, most of us, was if (ceftiofur) worked, if it’ll save a cow, we’ll spend the money,” Byron said. “You’re talking about a thousand-dollar animal or more.”

After the USDA found high traces of ceftiofur in the cow he’d sold for slaughter, Byron received a letter from the FDA warning him to improve his processes. The agency evaluated his operation later that year, found it to be in order and closed the case. The agencies took no other action.

Additional reporting by Mimi Dwyer in New York; edited by Blake Morrison and Michael Williams

Veterinarians face conflicting allegiances to animals, farmers - and drug companies

GATE KEEPER: Steven Henry, a swine specialist from Abilene, Kansas, says sales pressure from the drug industry will remain high when veterinarians are put in charge of antibiotics in 2016. REUTERS/Dave Kaup

Part 3: The FDA is counting on vets to curb antibiotic use, but not even the government knows which of the animal doctors has financial ties to the pharmaceutical industry

NEW YORK – In 2016, a new U.S. Food and Drug Administration policy will give veterinarians a key role in combating a surge in antibiotic-resistant “superbugs” that infect humans. For the first time, the agency will require veterinarians, not farmers, to decide whenever antibiotics used by people are given to animals.

Medical doctors issue antibiotics by prescription only. Yet farmers and food companies have been able to buy the same or similar drugs over the counter to add to feed and water. The drugs not only help prevent disease but enable livestock to grow faster on less feed.

The new directive is meant to guard against the overuse of the drugs in American meat production. But by enlisting the help of veterinarians, a Reuters examination found, the FDA will be empowering a profession that not only has allegiances to animals, farmers and public health, but also has pervasive and undisclosed financial ties to the makers of the drugs.

The relationships between medical doctors and the pharmaceutical industry are subject to strict rules that require the public disclosure of payments for meals, trips, consulting, speaking and research.

No laws or regulations – including the new FDA directives –
require veterinarians to reveal financial connections to drug companies. That means veterinarians can be wined and dined and given scholarships, awards, stipends, gifts and trips by pharmaceutical benefactors without the knowledge of the FDA or the public.

Of the 90,000 veterinarians who practice in the United States, about 11,000 – or one of every eight – work in food animal production, according to a 2013 workforce study. Livestock and poultry specialists advise growers on health issues from insemination to birth to weaning to fattening to euthanasia. They also treat a variety of illnesses and injuries. Many train farmhands how to spot disease and administer drugs.

In some ways, the role of the veterinarian is more complicated than that of the medical doctor. For a veterinarian, the patient is the animal but the client is the owner. In the case of food production, those clients are seeking to maximize
profit, and part of the veterinarian’s job is to help them do so.

Veterinary medicine is a little-regulated corner of the medical profession, more dependent on industry funding than its human counterparts, and Reuters found that drug companies support veterinarians at every stage of their careers. Sometimes the payments are small – $10 for a meal or $250 for an hour’s talk. But larger funding arrangements – $100,000 for research, for example – are not uncommon.

Of the 22 veterinarians who advised the FDA in recent years on how to use antibiotics on farms, 11 received money from pharmaceutical companies. Many of these details weren’t disclosed by the FDA, which wasn’t required until 2007 to post on its website “the type, nature and magnitude of the financial interests” of its advisers. Reuters identified payments to FDA advisory group members by reviewing veterinary journals, industry publications, meeting transcripts, conference programs and resumes, among other sources.

The influence of drug companies also extends to the training that current and future veterinarians receive. For example, pharmaceutical companies routinely suggest topics and speakers for the continuing education events that veterinarians must attend to keep their licenses. Such involvement is forbidden in human medicine, according to the Accreditation Council for Continuing Medical Education.

The world’s largest animal-drug company, Zoetis, has also extended its reach into high schools: In 2011, the company gave $50,000 to help fund a weeklong Purdue University veterinary camp for 10th, 11th and 12th graders.

The American Veterinary Medical Association, the non-profit organization that represents the nation’s veterinarians, also benefits from contributions from the pharmaceutical industry. The association’s ethics code calls on veterinarians to divulge all potential conflicts of interests. But only after Reuters asked did the group disclose that it has accepted $3.3 million from drug companies over the past four years. It declined to say which pharmaceutical companies contributed to the group.

“I’m very concerned that the profession is poised to lose public trust,” said Michael Blackwell, a former deputy director of the FDA’s Center for Veterinary Medicine. “I don’t think we can gain public trust if the perception exists of a conflict of interest.”

Told of the Reuters findings, U.S. Rep. Louise Slaughter, D-N.Y., said she will introduce legislation to require public disclosure of drug company payments to veterinarians. Billions of dollars in payments to doctors have been disclosed under the Physician Payments Sunshine Act of 2010, but that law does not apply to veterinarians.

“That’s a terrible omission,” said Slaughter, a microbiologist who has led congressional efforts to reduce antibiotics in livestock. She said transparency is essential as veterinarians prepare to take an important new role for public health.


Today, about 80 percent of all antibiotics used in the United States go to food animals, mostly as part of the feed or water given to whole herds and flocks. Some of the antibiotics serve a dual purpose: They help control and prevent outbreaks of disease, and they affect microorganisms in the digestive system in ways that help animals gain weight more effectively with less feed.

Earlier this year, Reuters reported that some of America’s largest poultry firms were giving antibiotics to their flocks far more often than regulators knew. In most cases, the drugs were being administered at the low levels that are especially conducive to the growth of superbugs.

Scientists with the U.S. Centers for Disease Control and Prevention said antibiotic use contributes to resistance by killing weaker bacteria and enabling the strongest to survive and multiply. Each year, about 2 million people are sickened in the United States with infections resistant to antibiotics, the CDC estimates. At least 23,000 people die.

INJECTIBLE ANTIBIOTIC: Individual pigs may get Enroflox 100  if they appear to be getting sick. In 2005, the FDA banned a similar drug that was put in water for chickens. The concern: that it was promoting antibiotic-resistant Campylobacter. REUTERS/Duff Wilson

Yet even as health professionals have issued warnings, antibiotics use on U.S. farms increased by 16 percent from 2009 to 2012, the FDA reported in October.

That’s one of the reasons the FDA has turned to veterinarians. The plan is to have vets supervise the use of antibiotics that are important to fighting human illnesses, and to create a paper trail of when and where those drugs are used. Currently the government keeps only overall sales data on antibiotic use in animals.

“We want to bring that professional supervision into the process,” said Michael Taylor, FDA deputy commissioner for foods and veterinary medicine.

As veterinarians are asked to safeguard public health, the financial conflicts they face deserve greater scrutiny, said Daniel Carlat, who directed a project for the nonprofit Pew Charitable Trust that examined medical conflicts of interest.

“It hasn’t come up because people have not been as concerned about the health and welfare of animals as they have humans,” said Carlat, an associate clinical professor of psychiatry at Tufts Medical School.

“I think the issue is much more germane to the health of humans now, because we’re talking about antibiotic use in animals that we’re eating and that could potentially affect the effectiveness of antibiotics that we use for our own health,” Carlat said. “Suddenly, conflicts of interest in veterinary medicine have become quite relevant for humans… We need to know more.”


The typical starting income of a food-animal veterinarian is about $71,000 a year and grows to about $103,000, surveys show. Some treat dogs and cats, too. Many also sell medications in addition to services – a potential conflict that has been restricted in Denmark.

American veterinarians say that because there are no pharmacies that dispense animal drugs, their dual role as healers and distributors is a convenience, and what’s more, their drug profit margins are usually small. Drug companies also sell directly to the biggest livestock producers, and their direct-to-farmer advertising bypasses veterinarians entirely.

“I'm very concerned that the profession is poised to lose public trust. I don't think we can gain public trust if the perception exists of a conflict of interest.”

Michael Blackwell, former deputy director FDA Center for Veterinary Medicine

The best-paid veterinarians aren’t the ones treating animals. Rather, they work for drug companies. Veterinarians in pharmaceuticals, biotechnology, research and agrochemicals made on average  $167,000 a year in 2009, a salary survey shows. Zoetis, the leading animal drug maker, has 825 veterinary technical advisors and sales people in the United States. The company had about $1.3 billion in antibiotic drug sales in 2013 – 26 percent of its total revenue.

In addition to the vets that Zoetis employs directly, the company also has financial relationships with veterinarians across the nation. That includes providing scholarships and loan assistance for veterinary students, awards for faculty, sponsorship of continuing education sessions, funding for veterinary associations, and payments for veterinarians to speak, consult and research.

Zoetis won’t say which veterinarians it helps, or how many. Spokeswoman Elinore White said the company monitors its payments to veterinarians “to ensure that our educational and promotional efforts do not inappropriately reward prescribing or dispensing behavior.” She declined to discuss how the tracking system works or whether the company has identified any problematic overprescribing.

The upcoming FDA directive means that “now there will be a gatekeeper” between drug companies and food producers, said Steven Henry, a Kansas veterinarian advising farmers who raise 2 million pigs a year.

Henry and others predict that the new rules will do little to stanch the flow of antibiotics to farmers because drug companies need to maintain volumes and profits. “These impediments are going to restrict sales – until they figure out a way not to restrict sales,” Henry said of drug companies.

COW DOCTOR: Fred Gingrich, an Ashland, Ohio, veterinarian and incoming president of the American Association of Bovine Practitioners: “We welcome the responsibility and the discussion” around the use of antibiotics. REUTERS/Aaron Josefczyk

“The fact that they’re being supported by the companies they’re supposed to be overseeing raises issues about the impact of those payments.”

Eric Campbell, professor at Harvard University

Colorado cattle rancher Mike Callicrate said he expects veterinarians to follow the wishes of the ranchers who employ them. “These guys are going to fight to the death to keep their antibiotics,” Callicrate said of ranchers who operate the largest farms. What veterinarians end up prescribing, he said, “depends on who they’re getting paid by.”

Fred Gingrich, a veterinarian in Ashland, Ohio, and the incoming president of the American Association of Bovine Practitioners, said that was a cynical view of the ethics of veterinarians and growers. “I’m proud of what we do,” he said. “We welcome the responsibility and the discussion.”


In its guidance to veterinarians and the industry, the FDA is emphasizing the term “judicious use.” Medications should be used judiciously to prevent and treat specific diseases, not for promoting growth or feed efficiency, the agency says.

Craig Rowles, a veterinarian in Carroll, Iowa, and an owner of Elite Pork Partnership, said he has stopped using antibiotics to promote growth. Each year, Rowles sells 150,000 hogs to Tyson Foods. He said he still puts doses of tetracycline in the animal feed for two weeks shortly after weaning. That’s when the pigs are most vulnerable, he said, and the antibiotics help stave off infections. Rowles considers such doses a judicious use even if the pigs aren’t sick. “That’s fairly routine for us,” he said.

Two new voluntary rules, effective in December 2016 and supported by drug makers, prohibit using antibiotics to promote fattening animals for food, and require prescriptions for all antibiotics used in both animal and human medicine. But the new guidelines still permit antibiotics to be used for disease prevention, a provision that some health advocates say will enable veterinarians to rationalize almost any prescription.

The FDA’s handling of the antibiotics issue itself illustrates the conflicts facing the industry and the government.

The agency’s Veterinary Medicine Advisory Committee, for example, discussed the use of antibiotics four times between 1999 and 2006. Among the 22 veterinarians who participated in those discussions, half had some sort of financial tie with one or more of the companies that sold antibiotics. In the two most recent meetings, an even higher percentage, seven of 10, had financial ties to drug makers.

PIG MEDICINE: Craig Rowles a veterinarian in Carroll, Iowa, raises 150,000 hogs a year for Tyson Foods. He said he routinely gives the pigs antibiotics after weaning to protect against infection. REUTERS/Duff Wilson

Last year, the FDA dissolved the group, deeming the veterinary committee “no longer necessary because of other opportunities for input.”  Among those other opportunities is a task force formed by veterinary colleges. The members include Willie Reed, the dean at Purdue University’s veterinary school.

Purdue pays Reed $276,000 a year. In March, Zoetis named him to its board of directors. That position pays Reed $240,000 annually in cash and stock and requires directors to act in the fiduciary interest of the company. The task force announcement last month didn’t mention Reed’s tie to Zoetis.

Reed’s dual role creates “an ethical smog” because the veterinary school and dean could be perceived as too close to the interests of a single drug company, said Thomas Donaldson, professor of business ethics at the Wharton School of the University of Pennsylvania. The connection to Zoetis, he said, should have been disclosed prominently when the colleges set up the antibiotics task force. “That’s a no brainer,” Donaldson said. “You’ve got a tiger by the tail there.”

Reed declined to talk to Reuters directly, but issued a statement – through Zoetis.

“I have taken an oath as a veterinarian and make recommendations regarding animal health issues based on my scientific knowledge, experience and skills in order to protect human and animal health,” he said. “The role I play as a member of the Zoetis board is consistent with this oath.’”

Edited by Blake Morrison


Farmaceuticals: The drugs fed to farm animals and the risks posed to humans

By Brian Grow, P.J. Huffstutter, Michael Erman, Duff Wilson and Mimi Dwyer

Web programming: Charlie Szymanski

Data: Michael Erman

Graphics: Matthew Weber and Maryanne Murray

Photo editing: Jim Bourg

Design: Troy Dunkley

Editing: Blake Morrison and David Greising