US: E. Coli Path Shows Flaws in Beef Inspection

Stephanie Smith, a children's dance instructor, thought she had a
stomach virus. The aches and cramping were tolerable that first day,
and she finished her classes.

Then her diarrhea turned bloody. Her kidneys shut down. Seizures knocked her unconscious. The convulsions grew so relentless that doctors had to put her in a coma
for nine weeks. When she emerged, she could no longer walk. The
affliction had ravaged her nervous system and left her paralyzed.

Ms. Smith, 22, was found to have a severe form of food-borne illness caused by E. coli, which Minnesota officials traced to the hamburger that her mother had grilled for their Sunday dinner in early fall 2007.

"I ask myself every day, 'Why me?' and 'Why from a hamburger?' "Ms.
Smith said. In the simplest terms, she ran out of luck in a food-safety
game of chance whose rules and risks are not widely known.

Meat companies and grocers have been barred from selling ground beef
tainted by the virulent strain of E. coli known as O157:H7 since 1994,
after an outbreak at Jack in the Box restaurants left four children
dead. Yet tens of thousands of people are still sickened annually by
this pathogen, federal health officials estimate, with hamburger being
the biggest culprit. Ground beef has been blamed for 16 outbreaks in
the last three years alone, including the one that left Ms. Smith
paralyzed from the waist down. This summer, contamination led to the
recall of beef from nearly 3,000 grocers in 41 states.

Ms. Smith's reaction to the virulent strain of E. coli was extreme,
but tracing the story of her burger, through interviews and government
and corporate records obtained by The New York Times, shows why eating
ground beef is still a gamble. Neither the system meant to make the
meat safe, nor the meat itself, is what consumers have been led to
believe.

Ground beef is usually not simply a chunk of meat run through a
grinder. Instead, records and interviews show, a single portion of
hamburger meat is often an amalgam of various grades of meat from
different parts of cows and even from different slaughterhouses. These
cuts of meat are particularly vulnerable to E. coli contamination, food
experts and officials say. Despite this, there is no federal
requirement for grinders to test their ingredients for the pathogen.

The frozen hamburgers that the Smiths ate, which were made by the
food giant Cargill, were labeled "American Chef's Selection Angus Beef
Patties." Yet confidential grinding logs and other Cargill records show
that the hamburgers were made from a mix of slaughterhouse trimmings
and a mash-like product derived from scraps that were ground together
at a plant in Wisconsin. The ingredients came from slaughterhouses in
Nebraska, Texas and Uruguay, and from a South Dakota company that
processes fatty trimmings and treats them with ammonia to kill bacteria.

Using a combination of sources - a practice followed by most large
producers of fresh and packaged hamburger - allowed Cargill to spend
about 25 percent less than it would have for cuts of whole meat.

Those low-grade ingredients are cut from areas of the cow that are
more likely to have had contact with feces, which carries E. coli,
industry research shows. Yet Cargill, like most meat companies, relies
on its suppliers to check for the bacteria and does its own testing
only after the ingredients are ground together. The United States
Department of Agriculture, which allows grinders to devise their own
safety plans, has encouraged them to test ingredients first as a way of
increasing the chance of finding contamination.

Unwritten agreements between some companies appear to stand in the
way of ingredient testing. Many big slaughterhouses will sell only to
grinders who agree not to test their shipments for E. coli, according
to officials at two large grinding companies. Slaughterhouses fear that
one grinder's discovery of E. coli will set off a recall of ingredients
they sold to others.

"Ground beef is not a completely safe product," said Dr. Jeffrey Bender, a food safety expert at the University of Minnesota
who helped develop systems for tracing E. coli contamination. He said
that while outbreaks had been on the decline, "unfortunately it looks
like we are going a bit in the opposite direction."

Food scientists have registered increasing concern about the
virulence of this pathogen since only a few stray cells can make
someone sick, and they warn that federal guidance to cook meat
thoroughly and to wash up afterward is not sufficient. A test by The
Times found that the safe handling instructions are not enough to
prevent the bacteria from spreading in the kitchen.

Cargill, whose $116.6 billion in revenues last year made it the
country's largest private company, declined requests to interview
company officials or visit its facilities. "Cargill is not in a
position to answer your specific questions, other than to state that we
are committed to continuous improvement in the area of food safety,"
the company said, citing continuing litigation.

The meat industry treats much of its practices and the ingredients
in ground beef as trade secrets. While the Department of Agriculture
has inspectors posted in plants and has access to production records,
it also guards those secrets. Federal records released by the
department through the Freedom of Information Act blacked out details of Cargill's grinding operation that could be learned only through copies of the documents
obtained from other sources. Those documents illustrate the restrained
approach to enforcement by a department whose missions include ensuring
meat safety and promoting agriculture markets.

Within weeks of the Cargill outbreak in 2007, U.S.D.A. officials
swept across the country, conducting spot checks at 224 meat plants to
assess their efforts to combat E. coli. Although inspectors had been
monitoring these plants all along, officials found serious problems at 55 that were failing to follow their own safety plans.

"Every time we look, we find out that things are not what we hoped
they would be," said Loren D. Lange, an executive associate in the
Agriculture Department's food safety division.

In the weeks before Ms. Smith's patty was made, federal inspectors had repeatedly found that Cargill was violating its own safety procedures
in handling ground beef, but they imposed no fines or sanctions,
records show. After the outbreak, the department threatened to withhold
the seal of approval that declares "U.S. Inspected and Passed by the
Department of Agriculture."

In the end, though, the agency accepted Cargill's proposal to
increase its scrutiny of suppliers. That agreement came early last year
after contentious negotiations, records show. When Cargill defended its
safety system and initially resisted making some changes, an agency official wrote back: "How is food safety not the ultimate issue?"

The Risk

On Aug. 16, 2007, the day Ms. Smith's hamburger was made, the No.3 grinder
at the Cargill plant in Butler, Wis., started up at 6:50 a.m. The
largest ingredient was beef trimmings known as "50/50" - half fat, half
meat - that cost about 60 cents a pound, making them the cheapest component.

Cargill bought these trimmings - fatty edges sliced from better cuts
of meat - from Greater Omaha Packing, where some 2,600 cattle are
slaughtered daily and processed in a plant the size of four football
fields.

As with other slaughterhouses, the potential for contamination is
present every step of the way, according to workers and federal
inspectors. The cattle often arrive with smears of feedlot feces that
harbor the E. coli pathogen, and the hide must be removed carefully to
keep it off the meat. This is especially critical for trimmings sliced
from the outer surface of the carcass.

Federal inspectors based at the plant are supposed to monitor the
hide removal, but much can go wrong. Workers slicing away the hide can
inadvertently spread feces to the meat, and large clamps that hold the
hide during processing sometimes slip and smear the meat with feces,
the workers and inspectors say.

Greater Omaha vacuums and washes carcasses with hot water and lactic
acid before sending them to the cutting floor. But these safeguards are
not foolproof.

"As the trimmings are going down the processing line into combos or
boxes, no one is inspecting every single piece," said one federal
inspector who monitored Greater Omaha and requested anonymity because
he was not authorized to speak publicly.

The E. coli risk is also present at the gutting station, where intestines are removed, the inspector said

Every five seconds or so, half of a carcass moves into the
meat-cutting side of the slaughterhouse, where trimmers said they could
keep up with the flow unless they spot any remaining feces.

"We would step in and stop the line, and do whatever you do to take
it off," said Esley Adams, a former supervisor who said he was fired
this summer after 16 years following a dispute over sick leave. "But
that doesn't mean everything was caught."

Two current employees said the flow of carcasses keeps up its torrid
pace even when trimmers get reassigned, which increases pressure on
workers. To protest one such episode, the employees said, dozens of
workers walked off the job for a few hours earlier this year. Last
year, workers sued Greater Omaha, alleging that they were not paid for
the time they need to clean contaminants off their knives and other
gear before and after their shifts. The company is contesting the
lawsuit.

Greater Omaha did not respond to repeated requests to interview
company officials. In a statement, a company official said Greater
Omaha had a "reputation for embracing new food safety technology and
utilizing science to make the safest product possible."

The Trimmings

In making hamburger meat, grinders aim for a specific fat content -
26.6 percent in the lot that Ms. Smith's patty came from, company
records show. To offset Greater Omaha's 50/50 trimmings, Cargill added
leaner material from three other suppliers.

Records show that some came from a Texas slaughterhouse, Lone Star
Beef Processors, which specializes in dairy cows and bulls too old to
be fattened in feedlots. In a form letter
dated two days before Ms. Smith's patty was made, Lone Star recounted
for Cargill its various safety measures but warned "to this date there
is no guarantee for pathogen-free raw material and we would like to
stress the importance of proper handling of all raw products."

Ms. Smith's burger also contained trimmings from a slaughterhouse in
Uruguay, where government officials insist that they have never found
E. coli O157:H7 in meat. Yet audits of Uruguay's meat operations
conducted by the U.S.D.A. have found sanitation problems, including
improper testing for the pathogen. Dr. Hector J. Lazaneo, a meat safety
official in Uruguay, said the problems were corrected immediately.
"Everything is fine, finally," he said. "That is the reason we are
exporting."

Cargill's final source was a supplier that turns fatty trimmings
into what it calls "fine lean textured beef." The company, Beef
Products Inc., said it bought meat that averages between 50 percent and
70 percent fat, including "any small pieces of fat
derived from the normal breakdown of the beef carcass." It warms the
trimmings, removes the fat in a centrifuge and treats the remaining
product with ammonia to kill E. coli.

With seven million pounds produced each week, the company's product
is widely used in hamburger meat sold by grocers and fast-food
restaurants and served in the federal school lunch program. Ten percent
of Ms. Smith's burger came from Beef Products, which charged Cargill
about $1.20 per pound, or 20 cents less than the lean trimmings in the
burger, billing records show.

An Iowa State University study
financed by Beef Products found that ammonia reduces E. coli to levels
that cannot be detected. The Department of Agriculture accepted the
research as proof that the treatment was effective and safe. And
Cargill told the agency after the outbreak that it had ruled out Beef Products as the possible source of contamination.

But federal school lunch officials found E. coli in Beef Products
material in 2006 and 2008 and again in August, and stopped it from
going to schools, according to Agriculture Department records and
interviews. A Beef Products official, Richard Jochum, said that last
year's contamination stemmed from a "minor change in our process,"
which the company adjusted. The company did not respond to questions
about the latest finding.

In combining the ingredients, Cargill was following a common
industry practice of mixing trim from various suppliers to hit the
desired fat content for the least money, industry officials said.

In all, the ingredients for Ms. Smith's burger cost Cargill about $1
a pound, company records show, or about 30 cents less than industry
experts say it would cost for ground beef made from whole cuts of meat.

Ground beef sold by most grocers is made from a blend of
ingredients, industry officials said. Agriculture Department
regulations also allow hamburger meat labeled ground chuck or sirloin
to contain trimmings from those parts of the cow. At a chain like Publix Super Markets,
customers who want hamburger made from whole cuts of meat have to buy a
steak and have it specially ground, said a Publix spokeswoman, Maria
Brous, or buy a product like Bubba Burgers, which boasts on its
labeling, "100% whole muscle means no trimmings."

To finish off the Smiths' ground beef, Cargill added bread crumbs
and spices, fashioned it into patties, froze them and packed them 18 to
a carton.

The listed ingredients revealed little of how the meat was made. There was just one meat product listed: "Beef."

Tension Over Testing

As it fed ingredients into its grinders, Cargill watched for some
unwanted elements. Using metal detectors, workers snagged stray nails
and metal hooks that could damage the grinders, then warned suppliers
to make sure it did not happen again.

But when it came to E. coli O157:H7, Cargill did not screen the
ingredients and only tested once the grinding was done. The potential
pitfall of this practice surfaced just weeks before Ms. Smith's patty
was made. A company spot check in May 2007 found E. coli in finished
hamburger, which Cargill disclosed
to investigators in the wake of the October outbreak. But Cargill told
them it could not determine which supplier had shipped the tainted meat
since the ingredients had already been mixed together.

"Our finished ground products typically contain raw materials from
numerous suppliers," Dr. Angela Siemens, the technical services vice
president for Cargill's meat division, wrote
to the U.S.D.A. "Consequently, it is not possible to implicate a
specific supplier without first observing a pattern of potential
contamination."

Testing has been a point of contention since the 1994 ban on selling
ground beef contaminated with E. coli O157:H7 was imposed. The
department moved to require some bacterial testing of ground beef, but
the industry argued that the cost would unfairly burden small
producers, industry officials said. The Agriculture Department opted to
carry out its own tests for E. coli, but it acknowledges that its
15,000 spot checks a year at thousands of meat plants and groceries
nationwide is not meant to be comprehensive. Many slaughterhouses and
processors have voluntarily adopted testing regimes, yet they vary
greatly in scope from plant to plant.

The retail giant Costco is one of the few big producers that tests
trimmings for E. coli before grinding, a practice it adopted after a
New York woman was sickened in 1998 by its hamburger meat, prompting a
recall.

Craig Wilson, Costco's food safety director, said the company
decided it could not rely on its suppliers alone. "It's incumbent upon
us," he said. "If you say, 'Craig, this is what we've done,' I should
be able to go, 'Cool, I believe you.' But I'm going to check."

Costco said it had found E. coli in foreign and domestic beef
trimmings and pressured suppliers to fix the problem. But even Costco,
with its huge buying power, said it had met resistance from some big
slaughterhouses. "Tyson will not supply us," Mr. Wilson said. "They
don't want us to test."

A Tyson spokesman, Gary Mickelson, would not respond to Costco's
accusation, but said, "We do not and cannot" prohibit grinders from
testing ingredients. He added that since Tyson tests samples of its
trimmings, "we don't believe secondary testing by grinders is a
necessity."

The food safety officer at American Foodservice, which grinds 365
million pounds of hamburger a year, said it stopped testing trimmings a
decade ago because of resistance from slaughterhouses. "They would not
sell to us," said Timothy P. Biela, the officer. "If I test and it's
positive, I put them in a regulatory situation. One, I have to tell the
government, and two, the government will trace it back to them. So we
don't do that."

The surge in outbreaks since 2007 has led to finger-pointing within the industry.

Dennis R. Johnson, a lobbyist for the largest meat processors, has
said that not all slaughterhouses are looking hard enough for
contamination. He told U.S.D.A. officials last fall that those with
aggressive testing programs typically find E. coli in as much as 1
percent to 2 percent of their trimmings, yet some slaughterhouses
implicated in outbreaks had failed to find any.

At the same time, the meat processing industry has resisted taking
the onus on itself. An Agriculture Department survey of more than 2,000
plants taken after the Cargill outbreak showed that half of the
grinders did not test their finished ground beef for E. coli; only 6
percent said they tested incoming ingredients at least four times a
year.

In October 2007, the agency issued a notice recommending that
processors conduct at least a few tests a year to verify the testing
done by slaughterhouses. But after resistance from the industry, the
department allowed suppliers to run the verification checks on their
own operations.

In August 2008, the U.S.D.A. issued a draft guideline
again urging, but not ordering, processors to test ingredients before
grinding. "Optimally, every production lot should be sampled and tested
before leaving the supplier and again before use at the receiver," the
draft guideline said.

But the department received critical comments on the guideline,
which has not been made official. Industry officials said that the cost
of testing could unfairly burden small processors and that
slaughterhouses already test. In an October 2008 letter to the
department, the American Association of Meat Processors said the
proposed guideline departed from U.S.D.A.'s strategy of allowing
companies to devise their own safety programs, "thus returning to more
of the agency's 'command and control' mind-set."

Dr. Kenneth Petersen, an assistant administrator with the
department's Food Safety and Inspection Service, said that the
department could mandate testing, but that it needed to consider the
impact on companies as well as consumers. "I have to look at the entire
industry, not just what is best for public health," Dr. Petersen said.

Tracing the Illness

The Smiths were slow to suspect the hamburger. Ms. Smith ate a mostly vegetarian diet,
and when she grew increasingly ill, her mother, Sharon, thought the
cause might be spinach, which had been tied to a recent E. coli
outbreak.

Five days after the family's Sunday dinner, Ms. Smith was admitted
to St. Cloud Hospital in excruciating pain. "I've had women tell me
that E. coli is more painful than childbirth," said Dr. Phillip I.
Tarr, a pathogen expert at Washington University in St. Louis.

The vast majority of E. coli illnesses resolve themselves without complications, according to the Centers for Disease Control and Prevention.
Five percent to 10 percent develop into a condition called hemolytic
uremic syndrome, which can affect kidney function. While most patients
recover, in the worst cases, like Ms. Smith's, the toxin in E. coli
O157:H7 penetrates the colon wall, damaging blood vessels and causing
clots that can lead to seizures.

To control Ms. Smith's seizures, doctors put her in a coma and flew her to the Mayo Clinic, where doctors worked to save her.

"They didn't even think her brain would work because of the
seizuring," her mother said. "Thanksgiving Day, I was sitting there
holding her hand when a group of doctors came in, and one looked at me
and just walked away, with nothing good to say. And I said, 'Oh my God,
maybe this is my last Thanksgiving with her,' and I stayed and prayed."

Ms. Smith's illness was linked to the hamburger only by chance. Her
aunt still had some of the frozen patties, and state health officials
found that they were contaminated with a powerful strain of E. coli
that was genetically identical to the pathogen that had sickened other
Minnesotans.

Dr. Kirk Smith, who runs the state's food-borne illness outbreak
group and is not related to Ms. Smith, was quick to finger the source.
A 4-year-old had fallen ill three weeks earlier, followed by her
year-old brother and two more children, state records show. Like Ms.
Smith, the others had eaten Cargill patties bought at Sam's Club, a
division of Wal-Mart.

Moreover, the state officials discovered that the hamburgers were
made on the same day, Aug. 16, 2007, shortly before noon. The time
stamp on the Smiths' box of patties was 11:58.

On Friday, Oct. 5, 2007, a Minnesota Health Department warning led
local news broadcasts. "We didn't want people grilling these things
over the weekend," Dr. Smith said. "I'm positive we prevented
illnesses. People sent us dozens of cartons with patties left. It was
pretty contaminated stuff."

Eventually, health officials tied 11 cases of illness in Minnesota
to the Cargill outbreak, and altogether, federal health officials
estimate that the outbreak sickened 940 people. Four of the 11
Minnesota victims developed hemolytic uremic syndrome - an unusually
high rate of serious complications.

In the wake of the outbreak, the U.S.D.A. reminded consumers on its
Web site that hamburgers had to be cooked to 160 degrees to be sure any
E. coli is killed and urged them to use a thermometer to check the
temperature. This reinforced Sharon Smith's concern that she had
sickened her daughter by not cooking the hamburger thoroughly.

But the pathogen is so powerful that her illness could have started
with just a few cells left on a counter. "In a warm kitchen, E. coli
cells will double every 45 minutes," said Dr. Mansour Samadpour, a
microbiologist who runs IEH Laboratories in Seattle, one of the meat
industry's largest testing firms.

With help from his laboratories, The Times prepared three pounds of
ground beef dosed with a strain of E. coli that is nonharmful but acts
in many ways like O157:H7. Although the safety instructions on the
package were followed, E. coli remained on the cutting board even after
it was washed with soap. A towel picked up large amounts of bacteria
from the meat.

Dr. James Marsden, a meat safety expert at Kansas State University
and senior science adviser for the North American Meat Processors
Association, said the Department of Agriculture needed to issue better
guidance on avoiding cross-contamination, like urging people to use bleach
to sterilize cutting boards. "Even if you are a scientist, much less a
housewife with a child, it's very difficult," Dr. Marsden said.

Told of The Times's test, Jerold R. Mande, the deputy under
secretary for food safety at the U.S.D.A., said he planned to "look
very carefully at the labels that we oversee."

"They need to provide the right information to people," Mr. Mande said, "in a way that is readable and actionable."

Dead Ends

With Ms. Smith lying comatose in the hospital and others ill around
the country, Cargill announced on Oct. 6, 2007, that it was recalling
844,812 pounds of patties. The mix of ingredients in the burgers made
it almost impossible for either federal officials or Cargill to trace
the contamination to a specific slaughterhouse. Yet after the outbreak,
Cargill had new incentives to find out which supplier had sent the
tainted meat.

Cargill got hit by multimillion-dollar claims from people who got sick.

Shawn K. Stevens, a lawyer in Milwaukee working for Cargill, began
investigating. Sifting through state health department records from
around the nation, Mr. Stevens found the case of a young girl in Hawaii
stricken with the same E. coli found in the Cargill patties. But
instead of a Cargill burger, she had eaten raw minced beef at a
Japanese restaurant that Mr. Stevens said he traced through a
distributor to Greater Omaha.

"Potentially, it could let Cargill shift all the responsibility,"
Mr. Stevens said. In March, he sent his findings to William Marler, a
lawyer in Seattle who specializes in food-borne disease cases and is
handling the claims against Cargill.

"Most of the time, in these outbreaks, it's not unusual when I point
the finger at somebody, they try to point the finger at somebody else,"
Mr. Marler said. But he said Mr. Stevens's finding "doesn't rise to the
level of proof that I need" to sue Greater Omaha.

It is unclear whether Cargill presented the Hawaii findings to
Greater Omaha, since neither company would comment on the matter. In
December 2007, in a move that Greater Omaha said was unrelated to the
outbreak, the slaughterhouse informed
Cargill that it had taken 16 "corrective actions" to better protect
consumers from E. coli "as we strive to live up to the performance
standards required in the continuation of supplier relationship with
Cargill."

Those changes included better monitoring of the production line,
more robust testing for E. coli, intensified plant sanitation and added
employee training.

The U.S.D.A. efforts to find the ultimate source of the
contamination went nowhere. Officials examined production records of
Cargill's three domestic suppliers, but they yielded no clues. The
Agriculture Department contacted Uruguayan officials, who said they
found nothing amiss in the slaughterhouse there.

In examining Cargill, investigators discovered that their own inspectors had lodged complaints
about unsanitary conditions at the plant in the weeks before the
outbreak, but that they had failed to set off any alarms within the
department. Inspectors had found "large amounts of patties on the
floor," grinders that were gnarly with old bits of meat, and a worker
who routinely dumped inedible meat on the floor close to a production
line, records show.

Although none were likely to have caused the contamination, federal
officials said the conditions could have exacerbated the spread of
bacteria. Cargill vowed to correct the problems. Dr. Petersen, the
federal food safety official, said the department was working to make
sure violations are tracked so they can be used "in real time to take
action."

The U.S.D.A. found that Cargill had not followed its own safety
program for controlling E. coli. For example, Cargill was supposed to
obtain a certificate from each supplier showing that their tests had
found no E. coli. But Cargill did not have a certificate for the
Uruguayan trimmings used on the day it made the burgers that sickened
Ms. Smith and others.

After four months of negotiations, Cargill agreed to increase its
scrutiny of suppliers and their testing, including audits and periodic
checks to determine the accuracy of their laboratories.

A recent industry test in which spiked samples of meat were sent to
independent laboratories used by food companies found that some missed
the E. coli in as many as 80 percent of the samples.

Cargill also said it would notify suppliers whenever it found E.
coli in finished ground beef, so they could check their facilities. It
also agreed to increase testing of finished ground beef, according to a
U.S.D.A. official familiar with the company's operations, but would not
test incoming ingredients.

Looking to the Future

The spate of outbreaks in the last three years has increased pressure on the Agriculture Department and the industry.

James H. Hodges, executive vice president of the American Meat
Institute, a trade association, said that while the outbreaks were
disconcerting, they followed several years during which there were
fewer incidents. "Are we perfect?" he said. "No. But what we have done
is to show some continual improvement."

Dr. Petersen, the U.S.D.A. official, said the department had
adopted additional procedures, including enhanced testing at
slaughterhouses implicated in outbreaks and better training for
investigators.

"We are not standing still when it comes to E. coli," Dr. Petersen said.

The department has held a series of meetings since the recent
outbreaks, soliciting ideas from all quarters. Dr. Samadpour, the
laboratory owner, has said that "we can make hamburger safe," but that
in addition to enhanced testing, it will take an aggressive use of
measures like meat rinses and safety audits by qualified experts.

At these sessions, Felicia Nestor, a senior policy analyst with the
consumer group Food and Water Watch, has urged the government to
redouble its effort to track outbreaks back to slaughterhouses. "They
are the source of the problem," Ms. Nestor said.

For Ms. Smith, the road ahead is challenging. She is living at her
mother's home in Cold Spring, Minn. She spends a lot of her time in physical therapy,
which is being paid for by Cargill in anticipation of a legal claim,
according to Mr. Marler. Her kidneys are at high risk of failure. She
is struggling to regain some basic life skills and deal with the anger
that sometimes envelops her. Despite her determination, doctors say,
she will most likely never walk again.

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• 182 Health
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• 208 Regulation