Tracing the route of tainted spinach
How contaminated greens made their way from Central Coast to Midwest
January 1, 2007
The Daily Review
Ken McLaughlin and Brandon Bailey
As the mid-July sun bore down on California's central coast, automatic planters dropped millions of spinach seeds in a shimmering valley, where vegetable fields sit next to cattle pastures and a drowsy creek.
Just five weeks later and 2,000 miles away, a cosmetics distributor in suburban Milwaukee was enjoying a crisp green salad, her favorite lunch during the hot and muggy days of a Midwestern summer.
That health-conscious meal nearly killed her.
The story of how spinach put Lisa Brott in the hospital traces a complex journey from field to table that reveals the failure of the nation's produce industry to devise a reliable system for keeping one of its most popular products safe.
In the last decade, lettuce and spinach grown in California's central coast region have caused at least nine outbreaks of illness associated with E. coli bacteria. Today, fresh produce outpaces even meat as a source of food-borne illness. The beef industry tightened its safety practices after Jack In the Box burgers contaminated with E. coli killed four children in 1993, but with vegetables, regulators and growers are still catching up.
As health officials have urged Americans to eat more green, leafy vegetables, the produce industry has responded to consumers' unrelenting demand for convenience by giving them salad that's pre-washed and packaged in plastic. Yet the convenience may have a price: Some steps in processing might actually contribute to the spread of contamination.
Even after one of the biggest food-safety investigations in U.S. history, officials can only guess at what exactly caused the recent outbreak involving bagged fresh spinach, which killed three people and sickened 201 in 26 states and Canada.
Worse, they still can't guarantee that every salad will be safe to eat.
What they do know is the story began on a ranch in the central coast region, where half of the nation's leafy vegetables are grown. All the evidence points to one spinach field that no one will name, but many local growers suspect lies in a remote valley in San Benito County.
Planting the seeds
More and more growers are expanding inland into San Benito County, looking to grab a piece of the $3 billion in annual bagged salad sales. But cropland there is often interrupted by hills and — like the suspected farm — it is often invaded by feral pigs and other wild animals, and close to pastures with grazing livestock, which commonly carry E. coli.
Last July's temperatures in San Benito County were the hottest in years. But spinach thrives in warm — even hot — weather. It was time to plant.
Modern farmers have scheduling down to a science. They've devised computer spreadsheets to assure they supply processors and supermarket chains with a fixed amount of produce on a certain date, at a set price.
As the farmer planted that day, the biggest threats on his mind were probably insects, plant viruses and a virulent mold called Downey mildew.
"When E. coli showed up, it really blindsided all the spinach farmers," said Steve Remde, spinach supervisor for Dobler & Sons, a Watsonville firm whose fields are not suspected in the crisis.
Workers typically add soil amendments in the winter when nothing is growing. Those could include manure, but it is aged or composted to kill harmful bacteria, said Richard Smith at the University of California Cooperative Extension in Salinas.
The automatic planters pushed the tiny spinach seeds about a half-inch into beds 80 inches wide, perfectly aligned with the help of tractors guided by satellites circling the Earth.
It was the height of summer, so the spinach needed only 30 days to reach maturity. But in that time, a lot can happen.
Every morning, automated sprinklers moistened the soil as the seeds germinated, then every five to seven days as the plants grew. The heat meant the soil needed more water than usual, and University of California, Davis, food-safety scientist Dean Cliver suggests that water carried E.coli, even if tests did not detect it weeks later. The record heat provided an environment for bacteria on the plants to multiply faster, says Trevor Suslow, a food-safety researcher at UC Davis.
Most irrigation water in the area comes from wells, unregulated by any government agency. Farmers regularly test their well water for E. coli and other pathogens, but the tests are voluntary.
By the third week of August, farmworkers set out to harvest the spinach.
The leaves were a deep green by then, bursting with all the nutrients and anti-oxidants that make spinach such a healthy food.
But microscopic amounts of E. coli bacteria already could have nestled in the crevices of the leaves. Hunkering down, bacteria produce a slimy sheen that makes scrubbing it off difficult.
In the cool darkness before dawn, a band-saw blade on a mechanical harvester snipped the tops of the plants as the machine made its way down the emerald field, swallowing the
2- to 3-inch leaves — what produce marketers call "baby spinach."
The spinach then moved up the harvester's conveyer belt, blowing leaves over an air gap that forced rocks and anything heavier than the greens to the ground. Workers wearing hair nets and gloves filled plastic bins and stacked them like Legos in a flatbed truck.
For their own comfort and to prevent transfer of bacteria, farmworkers are supposed to have portable toilets and hand-washing facilities within a quarter mile of the field where they are working. But it's a rare day when state workplace inspectors actually check. Of the 77,000 farms in California, inspectors visit only about 1,000 a year.
Natural Selection Foods' 200,000-square-foot plant sits outside the historic town of San Juan Bautista amid fields of radicchio and other baby greens. The company has its own historic roots: Founded by University of California, Santa Cruz, alum Drew Goodman and his wife, Myra, a University of California, Berkeley, grad, Natural Selection was the first processing plant in the country to bag leafy greens for retail sale.
That was in 1986. Now, two decades later, federal officials say a troubling trend has emerged as the industry has grown: Since 1995, there have been 21 E. coli outbreaks involving spinach or lettuce. Of those that could be traced to a source, nine came from California's central coast region.
For eight months out of the year, the Natural Selections plant is abuzz with workers who look more like lab technicians than assembly line workers.
For the staff at the plant, the day begins at 6:30 a.m. with a chill.
Donning white smocks, hard hats, hair nets and latex gloves, they leave the summer weather behind, and entered a temperature-controlled plant where it averages 34 degrees. The uniforms are designed to ensure that the produce never makes contact with a worker's skin.
Workers wearing gloves examin the load for insect damage and mildew.
But in August no one tested for E. coli or other pathogens.
In less than 24 hours, forklift operators lifted the pallets into the next room, where workers remove rocks, moths, twigs and other foreign materials as the spinach moved up a conveyer belt. Whenever they leave the room, the workers dip their gloves and shoes in a cold chlorine-based solution.
Next, the spinach passed through a series of serpentine flumes, where the vegetable was sprayed, dunked and agitated in chilled, lightly chlorinated water.
The washing process is more thorough than anyone could do at home, but it still does not always reach into the crannies of every leaf. Even if it penetrates the protective sheen that develops around clumps of growing E. coli, the washing can miss some bacteria. In fact, the process of agitating the leaves while washing crushes some of them, releasing nutrient-rich moisture from within the leaf that could provide food for the bacteria to grow, Suslow says.
The washing kills 90 percent to 99 percent of the E. coli, says Mansour Samadpour, a microbiologist advising Natural Selection. "Which means that if you start with 10 million bacterial cells, you will end up with 100,000 to a million."
It takes only a few cells — together no wider than one-twentieth of a human hair — to make a person sick. This is where the price of convenience is sometimes paid. During processing, thousands of plants — often from different farms — are mixed together. Bacteria on just one leaf can smear onto dozens.
In the last processing steps, the spinach was dried in giant salad spinners, portioned out on computerized scales, then packed into bags at a rate of more than 100 a minute.
It was Aug. 15. The day shift was over.
Off to market
Natural Selection is known for organic salads, packaged under its Earthbound Farms label. But its plant also processes conventional leafy greens marketed under about 30 different brands. The implicated spinach was non-organic and packed in bags marked with the Dole label, then loaded onto refrigerated trucks.
For the next 2,000 miles, it was the truck driver — often an independent contractor — who was responsible for making sure the produce never reached temperatures higher than 45 degrees. There's little chance that E. coli will start here, but refrigeration keeps produce from wilting and inhibits the growth of dangerous bacteria.
Dole requires truckers to monitor cargo temperatures. But food-safety experts warn that a refrigerator unit could malfunction — or a driver might shut off a generator to save fuel — and no one might know.
The Dole spinach traveled from Northern California to the corporation's temperature-controlled regional depot in Springfield, Ohio. From there, it was trucked to a vast concrete building in the middle of a former Wisconsin cornfield.
The building — more than a million square feet divided into refrigerated and freezer rooms — is the distribution center for Milwaukee-based Roundy's Supermarkets, which owns grocery stores throughout Wisconsin, Illinois and Minnesota.
During the warm summer days, Lisa Brott liked nothing better than a big plate of greens for lunch.
She was 50 years old and life was good. She and her husband, John, married for 27 years, have two grown daughters living on their own.
She has a job she enjoys — selling beauty products out of her two-story home in a Milwaukee suburb — and time to sing in the choir at their Methodist church.
Lisa Brott avoided red meat and alcohol and worked out regularly at a nearby health club. During the summer, she bought a bag of fresh spinach almost every week.
She did most of her grocery shopping at Pick'n'Save stores — gleaming, well-stocked supermarkets that are part of the Roundy's chain. The one on Calhoun Road is near the homes of several customers. That's where she picked up a 6-ounce bag of Dole baby spinach Wednesday, Aug. 23.
During the week, her husband was at work as a sales executive for a manufacturing firm so she ate most of the spinach herself, munching on salads for lunch. Exactly a week later, she bought another bag at a different Pick'n'Save.
Cramps, then terror
On Saturday, Sept. 2, Brott was running errands when her stomach began to churn.
By Monday she had stomach cramps, so severe that she and her husband skipped a Labor Day barbecue at her brother's house. She figured she had the flu.
That night, the cramps were so painful that Brott decided she would see her doctor the next day. Morning brought a new alarm — bloody diarrhea.
Her mother drove her to the doctor's office, next door to Elmbrook Memorial Hospital.
Seeing how tired she was, staffers were worried enough to order a wheelchair and take her to the emergency room at the hospital. After several hours, a doctor ordered IV fluids because her diarrhea had left her dangerously dehydrated. Medical workers took blood and stool samples, but told her it would take 72 hours to get test results. They sent her home with no answers.
Brott had a second sleepless night, running to the bathroom every 15 minutes and doubling over from excruciating stomach pain. Then her diarrhea turned to pure blood. She was terrified.
She vomited. It must be cancer, she thought, and she began to cry.
Her husband was frantic. He thought she was hemorrhaging. He phoned doctors. He called an acquaintance on the hospital board. He called their minister, seeking comfort — or a referral.
They returned to the emergency room in the morning. Brott was admitted to the hospital, and by the next morning — Thursday — the doctors had test results: There were signs of E. coli.
Health workers started asking her questions. Brott remembered a client had brought some children to her house — the kids were raising rabbits and she wondered whether they had passed along an infection from the animals.
But Lisa Brott wasn't the only case of E. coli. By Friday, Sept. 8, the director of a hospital lab noticed several patients had stool samples that tested positive.
A blood bank manager reported an unusual demand for plasma to treat patients for a syndrome usually linked to the bacteria. Local health officials took notice.
Some officials suspected a children's petting zoo in upstate Wisconsin, which had been linked to an earlier E. coli illness.
As the weekend came and went, bagged spinach remained on the shelves of grocery stores across the nation.
That weekend, doctors told Brott the bad news: A severe kidney disorder was threatening her life.
Most E. coli is harmless to humans, but the deadly strain known as O157:H7 attacks the interior of the human intestinal tract, causing painful cramps and bloody diarrhea.
With some people, it stops there. But with Brott the infection had spread into her blood stream, damaging her red blood cells and clogging her kidneys. The bacteria threatened to interfere with her kidney function. This is known as hemolytic uremic syndrome, or HUS.
HUS can be fatal, especially for children and the elderly. Patients who survive are often vulnerable to kidney problems later.
Doctors put Brott in the hospital's intensive care unit. They ordered daily plasma transfusions, trying to counteract the damage ravaging her blood cells.
Every afternoon, a technician attached the apparatus to an incision in Lisa's Brott's neck. It took four hours to replace all of her plasma — up to 10 pints each time.
Sometimes her mother or husband would sit with her; sometimes she was alone in her single room, too tired to do anything but lie still.
She was exhausted, dazed by medication yet still in pain. One night, she had a panic attack. Distraught and shaking, Brott spent an hour and a half trying to persuade a nurse to let her go home.
On another night, her daughter prayed with her. Sarah Brott, 20, had taken the bus home from college in Madison, Wis. With her daughter at her side, Brott felt her fears lifting as she drifted off to sleep.
She was still in the hospital when her daughter returned to school, but she took comfort every day in a Biblical verse that Sarah Brott had written on a white board mounted on the otherwise bland wall of her hospital room.
"Those who hope in the Lord will renew their strength. They will soar on wings like eagles; they will run and not grow weary, they will walk and not be faint."
For eight days straight, the transfusions continued.
'It kept coming back to spinach'
Back at home, John Brott was fielding phone calls from Waukesha County public health investigators. He described their recent meals.
Like the other patients the investigators had interviewed, his wife had eaten baby spinach sold under the Dole brand at Pick'n'Save stores.
"It kept coming back to spinach," said Darren Rausch, an epidemiologist for Waukesha County, where Brookfield is located.
The empty spinach bags had been tossed out, but Brott had saved her itemized grocery receipts.
By Monday, Sept. 11, health officials in Wisconsin were comparing notes with federal authorities and counterparts in other states with similar cases.
Some officials were eager to go public. Others were concerned about making a mistake. Announcing that spinach was making people sick would cause growers and retailers to lose millions. By Wednesday, patient interviews in several states had implicated spinach. Yet there still was no scientific proof, no lab tests confirming any spinach was contaminated by E. coli.
The day passed, and there was no national warning.
But by the next day, when the FDA held a conference call with health officials from the affected states, the circumstantial evidence was overwhelming.
Of 50 patients whose illnesses had been reported so far nationwide, more than 80 percent had eaten bagged spinach. That was enough to convince Dr. David Acheson, a top medical officer at the FDA. He convened a news conference that evening to warn consumers not to eat bagged spinach.
That same night, corporate officials at Roundy's moved quickly, ordering all bagged spinach pulled from their store shelves. Other chains did the same.
Four days later, Brott was released from the hospital, as her blood and urine tests slowly returned toward healthy levels. But she remained weak. So much fluid had accumulated in her body during the time her kidneys weren't working that shoes wouldn't fit on her swollen feet.
For two more weeks, the normally vigorous woman needed a nap every afternoon. Doctors could not yet tell whether her kidneys had permanent damage.
But by late October she was feeling better. She decorated the front porch of her home with pumpkins and propped a whimsical scarecrow against the driveway light pole.
With medical expenses reaching $150,000, Brott signed on with Seattle attorney Bill Marler, who is handling nearly 100 claims related to the outbreak.
The health-conscious eater who used to buy a bag of spinach every week hasn't had any of the leafy green since. She's eager for news from the produce industry that things have changed.
She is not alone. Recent losses to the packaged salad industry are estimated at $100 million and climbing as some shoppers pass by packaged spinach, lettuce and other leafy vegetables.
The vast majority of U.S. produce is eaten without making anyone sick, of course. Bryan Aguirre, senior vice president of operations at Natural Selection, says he's confident that his company is doing everything it can to keep produce safe.
The firm, for instance, now routinely tests leafy greens entering the plant for salmonella and dangerous strains of E. coli.
Unlike the fields, the produce processing plants are subject to inspections from the state health department and U.S. Food and Drug Administration. In addition, Natural Selection is one of only a handful of vegetable processing plants in the country that take part in a food-safety program run by the U.S. Department of Agriculture, which includes surprise inspections.
But in the field, growers are still operating under voluntary guidelines that only now are getting closer scrutiny.
The packaged-salad industry, too, faces another sobering reality: With beef and poultry, E. coli and other pathogens are always destroyed by proper cooking. Salads are eaten raw.
The meat industry tightened its own procedures after the 1993 Jack in the Box outbreak. But with more consumers eating fruit and vegetables and the advent of high-volume processing of produce, federal officials are seeing a new trend: Outbreaks of E. coli contamination related to meat have decreased, while those related to fresh produce are rising.
Now, officials are investigating a new outbreak that they believe is related to shredded lettuce at Taco Bell restaurants in the Northeast.
All this has prompted growers and politicians to advocate stricter farming practices and better enforcement of existing rules. But substantial changes are years away. In fact, many food-safety experts suggest that irradiation is the only way to destroy harmful bacteria in raw produce. But the food industry has resisted the process because of the controversy over irradiated foods.
So salad lovers like Lisa Brott will never get 100 percent guarantees.
"There's no one silver bullet," Aguirre said. "You have to put a series of interventions in place and a series of steps to control and reduce your risk. And that's what we've done."
That's not enough for Brott. Health officials say spinach is now safe to eat, but she wants to hear that more is being done.
"It's scary," she said. "It doesn't make me comfortable at all."
More on this outbreak: Dole and Natural Selections Spinach E. coli Outbreak