How the FDA Works to Keep Produce Safe
By Michelle Meadows
The contamination of fresh spinach with the bacteria Escherichia coli (E. coli) O157:H7 during the fall of 2006 led to one of the largest and deadliest outbreaks of foodborne illness in recent years.
Most of the illnesses due to E. coli occurred from Aug. 26, 2006, to Sept. 16, 2006. Illnesses from spinach were confirmed in 26 states, and one case was confirmed in Ontario, Canada. In all, nearly 205 cases of illness were recorded during the outbreak, including 31 involving a type of kidney failure called hemolytic uremic syndrome (HUS). More than 100 people were hospitalized, and three deaths were recorded, including a 2-year-old boy in Idaho.
"One foodborne illness is too many," says Robert Brackett, Ph.D., director of the Food and Drug Administration's Center for Food Safety and Applied Nutrition (CFSAN). "We've seen that there is no such thing as a small error when it comes to produce safety. Even what may be perceived as a small error can have disastrous consequences."
Fresh produce is especially vulnerable to contamination because it's grown in a natural environment. It may be grown in a field or orchard, and it is often consumed raw, without cooking or other treatments that could destroy bacteria and other pathogens.
The FDA works with many partners to prevent contamination, but it's impossible to eliminate all problems through prevention. "When there is a problem, we want to catch it early and contain it through efficient outbreak response," says David Acheson, M.D., director of food safety and security in the CFSAN. "In this case, the FDA mounted a collaborative effort with public health authorities throughout the country to identify the source of the problem and prevent its spread."
The CFSAN has the lead responsibility for ensuring food safety, regulating everything except meat, poultry, and processed egg products, which are regulated by the U.S. Department of Agriculture (USDA). The Centers for Disease Control and Prevention (CDC) has a complementary role, serving as the lead federal agency for conducting disease surveillance and outbreak investigations. Surveillance systems coordinated by the CDC, in collaboration with the states, provide an essential early-information network to detect dangers in the food supply.
When a patient is diagnosed with E. coli O157:H7, a sample of the bacterial strain is sent to a participating PulseNet lab, says Christopher Braden, M.D., chief of outbreak response and surveillance at the CDC. PulseNet is a national network of public health laboratories that perform genetic fingerprinting on foodborne bacteria that result in human illness. Scientists use a process called pulsed-field gel electrophoresis (PFGE), a technique that subtypes bacteria.
"After the bacterial strain is subtyped or 'DNA fingerprinted' at a lab, the fingerprint is then uploaded electronically to the national PulseNet database where it can be compared with other patterns in other states," Braden says. "This gives us the capability to rapidly detect a cluster of infections with the same pattern occurring in multiple states. The strength of this system is its ability to identify patterns even if the affected people are geographically far apart."
Epidemiologists in Wisconsin were the first to alert CDC officials
about a small cluster of E. coli O157:H7 infections on Sept.
8, 2006. At that time, the source of the problem was unknown. Wisconsin
posted the bacterial strain to PulseNet to alert the entire network.
PulseNet confirmed that E. coli strains from infected patients
in Wisconsin had matching PFGE patterns and identified the same patterns
in other states.
"Once a cluster of cases with the same DNA pattern is identified, epidemiologists interview patients to determine whether cases of illness are linked to a food source or what other exposures they have in common," Braden says.
Oregon's state health department also had noted a small cluster
of cases and began interviewing patients. On Sept. 13, 2006, Wisconsin
and Oregon health officials both notified the CDC that eating fresh
spinach was reported. Most of those interviewed reported eating prepackaged
raw spinach that came from a bag.
That same day, the CDC Director's Emergency Operations Center notified the FDA's Emergency Operations Center (EOC) of the possible association of prepackaged raw spinach to the illnesses. The FDA's EOC is the agency's focal point for coordinating and managing all emergencies involving products regulated by the FDA.
After learning from the CDC that fresh spinach was confirmed as the source of the outbreak, the FDA immediately took action to prevent further illness by alerting the public. On Sept. 14, 2006, the FDA and the CDC held a conference call with the states and issued a public alert, advising consumers not to eat bagged spinach at that time. Neither frozen nor canned spinach was implicated in the outbreak.
Those who had become ill reported eating various brands of bagged spinach, processed by Natural Selection Foods LLC of San Juan Bautista, Calif. One week after Wisconsin officials notified the CDC, Natural Selections, which bags spinach under several brand names, announced a voluntary recall. The company recalled all spinach products with a date code of Oct. 1 or earlier. Five more companies issued recalls between Sept. 15 and Sept. 22. "These secondary recalls occurred because Natural Selections had shipped spinach to other companies that repackaged it," Acheson says.
The companies that issued secondary recalls were RLB Food Distributors, L.P., of West Caldwell, N.J.; River Ranch Fresh Foods LLC of Salinas, Calif.; Kenter Canyon Farms Inc. of Sun Valley, Calif.; Triple B Corp., doing business as S.T. Produce of Seattle; and Pacific Coast Fruit Co. of Portland, Ore.
On Sept. 16, the FDA expanded its warning and advised consumers not to eat any fresh spinach or fresh spinach-containing products. "We expanded the advisory when we learned that bagged spinach was sometimes sold in an un-bagged form at the retail level," Brackett says. The FDA advised retailers and food service operators that they should not sell raw spinach or blends that may contain raw spinach.
"We were also concerned about fresh spinach products that could still be in consumers' refrigerators," Brackett says. "At that point, the priority was to prevent further illnesses. We wanted to get the word out and get fresh spinach off the shelves while we conducted an investigation to narrow down the source. The number of illnesses was increasing daily, which was alarming. And the reach was nationwide. We also knew that there were a significant number of severe illnesses and hospitalizations."
E. coli O157:H7 causes diarrhea, often with bloody stools. Though most people recover in a week, some are more vulnerable, especially very young children and older people. Of the 95 cases that had been reported by Sept. 15, 2006, almost half had been hospitalized, and 15 percent had HUS, a condition that can cause kidney damage and death.
The FDA's advice to not eat any fresh spinach remained in effect until Sept. 22, 2006, Brackett says, when the FDA became confident that the source of the tainted spinach was restricted to three California counties. On that day, the FDA advised the public that fresh spinach implicated in the outbreak was grown in Monterey, San Benito, and Santa Clara Counties. At the same time, the FDA said that spinach grown elsewhere was not implicated in the outbreak and could be consumed.
From the first indications that fresh spinach was the culprit in the fall 2006 outbreak, investigators from the FDA, the CDC, and the states worked together to trace the implicated spinach back from consumption to the fields. The fact that illnesses were reported in multiple states suggested that contamination likely happened early in the distribution chain.
"Traceability to the farm is absolutely critical," says Jeff Farrar, D.V.M., Ph.D., chief of the Food and Drug Branch in the California Department of Health Services (CDHS). "We have seen many processors in the past who believed they had state-of-the-art traceability systems and when outbreaks occur, they realize their systems are not nearly as good as they thought."
On Sept. 14, 2006, Erica Pomeroy, an investigator in the San Francisco District of the FDA's Office of Regulatory Affairs, was already in the Salinas Valley with James Sigl, a senior investigator with the CDHS. The Salinas Valley is in the central coast region of California, about 55 miles south of San Jose and 20 miles northeast of Monterey.
"We were there conducting an assessment of a grower when we got a call that we needed to go to Natural Selections to start an investigation," Pomeroy says. They were in the area as part of the FDA's Lettuce Safety Initiative, which calls for assessments of growing and harvesting practices in major growing areas of leafy greens during September and October—months when outbreaks have occurred in the past. It took Pomeroy and Sigl about 45 minutes to drive to Natural Selections, where they reviewed the spinach washing and packaging process and collected documents from the company to determine which fields should be investigated.
Serving as team leaders for the investigation, they set up a command center at a hotel near the Salinas Valley. They were soon joined by other members of the California Food Emergency Response Team (CalFERT), a collaboration between the FDA's Pacific Region and the CDHS. CalFERT includes a diverse team of investigators, food scientists, environmental scientists, microbiologists, and chemists.
"Having the right people with the right skills available on site is critical to any successful investigation," says Barbara Cassens, the FDA's San Francisco district director. "By training the CalFERT staff together and offering them an opportunity to develop a working relationship prior to an emergency, we were able to move quickly in this outbreak response."
Pomeroy says the command center served as a place where they could have computer access and convene to share information, review findings, and plan strategies. "By focusing on fields associated with certain production lots, we were able to narrow the search to nine different ranches in the area," Pomeroy says. "We interviewed harvesters and growers about growing practices, irrigation practices, and their workers. We collected samples in and around the suspect fields from every possible source of contamination—water, soil, and domestic and wild animal feces." Labs of the FDA, the CDHS, and the USDA were able to process about 900 samples in a relatively short time.
And while investigators were conducting investigations on the farm level, other experts continued to analyze data collected in spinach questionnaires of people who had gotten ill. "The FDA collaborated with CDC to design a spinach questionnaire, a tool used to elicit a detailed history of spinach consumption from people who became ill," says Karl Klontz, M.D., a medical officer in the CFSAN. "We worked with CDC to analyze data collected using information such as brand name, date of purchase, Universal Product Code (UPC) code, and lot numbers."
On Sept. 20, 2006, a big break came when New Mexico's public health laboratory announced that it had isolated the outbreak's strain of E. coli O157:H7 from an open package of spinach that came from the refrigerator of a patient who had become ill. "The package of spinach that tested positive was Dole baby spinach best if used by August 30," Klontz says. This was a tremendous help in tracing back to the fields. Later, the strain implicated in the outbreak also was isolated from open packages of fresh spinach consumed by ill people in several other states, including Utah, Pennsylvania, Colorado, Ohio, and Wisconsin.
In the end, the focus of the trace-back investigation narrowed to four fields on four different ranches. On Sept. 29, 2006, the FDA announced that all spinach implicated in the outbreak traced back to Natural Selection Foods.
The investigation into how the spinach may have become contaminated included sample collection in facilities and a review of animal management practices, processing practices, and water use. Richard Gelting, Ph.D., an environmental engineer from the CDC's National Center for Environmental Health, was deployed to California at the FDA's request to join in the investigation of possible environmental sources of contamination. He investigated irrigation well structure, ground water movement, and water management practices in the implicated farm regions.
On Oct. 12, 2006, the FDA and the state of California announced test results. The field investigation discovered the same strain of E. coli O157:H7 involved in the illnesses in environmental samples collected at one of four implicated ranches that supplied spinach to Natural Selection. The samples included water from a stream and cattle feces taken from pasture areas on the ranch outside the crop fields. The E. coli O157:H7 isolates from these samples were matched to the outbreak strain by their PFGE patterns. Wild pig feces collected by investigators on the ranch were also found to contain this same strain of E. coli O157:H7.
"One unusual finding on the ranch was a high population of wild pigs," says Farrar. "But we haven't determined conclusively that wild pigs were the source of the contamination. Finding an exact-matching E. coli strain on an implicated farm is a first in California, and it directly reflects the CALFERT approach. But we still don't know how the pathogen came into contact with the spinach."
Fencing around the cow pastures nearby appears to keep the cows from going into the spinach fields. But Gerald Wiscomb, an expert on the team from the USDA's Wildlife Services, observed during his behavioral studies that pigs go into the crop fields on the ranch. "There are many possibilities," Pomeroy says. "It could be that the pigs rooted around the cow feces, contaminating themselves, and then later defecated in the spinach fields." Another possibility is that surface contamination from pig and cow feces in the pasture areas got into the ground water.
More research is needed to better understand how E. coli O157:H7 is introduced into the environment, says Farrar. "We need a better understanding of how the organism survives, whether it grows in certain conditions, exactly how it comes into contact with ready-to-eat products, and how it's affected by current processing practices," he says.
Produce-related outbreaks have been a continuing problem in recent years. Since 1995, there have been 20 outbreaks involving leafy greens, most traced to California. Many, but not all, were traced to the Salinas Valley. But there aren't definitive answers as to why many of these outbreaks are linked to the Salinas Valley, according to experts.
"Some have speculated that the reason other areas have not been implicated is simply because of the difference in the volume of production," Farrar says. "The Salinas Valley produces much more leafy greens than any other area in the country so we may be more likely to see outbreaks from this area. Others believe there are one or more unidentified geographic, topographic, or environmental risk factors unique to Salinas Valley that result in systemic contamination with E. coli O157:H7."
In a recent multiagency investigation project, the CDHS discovered many E. coli O157:H7 positive findings in agricultural ditch water in many area locations. This is the runoff water originating in the hills surrounding the Salinas Valley. Although none of these isolates have matched any known outbreak strains, these findings have resulted in a grant from the USDA's Agricultural Research Service to the University of California at Davis (UC-Davis) and the CDHS to look further into environmental sources of contamination in this area.
In 2004 and 2005, the FDA wrote to industry to express both the agency's concerns with continuing outbreaks and its expectations for industry to improve produce safety. One letter to the lettuce and tomato industries in February 2004 encouraged industry to review practices in light of the FDA's Good Agricultural Practices (GAPs) and Good Manufacturing Practices (GMPs) guidance. Another letter, sent in November 2005, reiterated this concern and focused on fresh-cut lettuce and other leafy greens.
After the most recent spinach outbreak, the FDA and the state of California asked the produce industry to develop a comprehensive plan to minimize the risk of another outbreak due to E. coli in spinach grown in California.
The Grower-Shipper Association of Central California, the Produce Marketing Association, the United Fresh Produce Association, and the Western Growers Association pledged their commitment and submitted a draft plan to the FDA.
Implementation of this plan is voluntary, but the FDA and the state of California may institute regulatory requirements if it is determined that they are needed.
The Public Health Service Act authorizes the FDA to make and enforce regulations to prevent the introduction, transmission, or spread of communicable disease. And the Federal Food, Drug, and Cosmetic Act provides a broad statutory framework for federal regulation to prevent adulterated foods from entering commerce, and to ensure that human food will not be hazardous to health.
Farrar says that industry also has proposed the creation of a statutorily based "Marketing Order and Marketing Agreement" on the state level for growers and processors as a possible avenue. "We are familiarizing ourselves with this proposal for mandatory and uniform standards for leafy greens industry in California that would be administered under the California Department of Agriculture's statutory authority," he says.
The FDA and the state of California have reiterated previous concerns and advised firms to review their operations in light of the FDA's guidance for minimizing microbial food safety hazards, as well as other available information regarding the reduction or elimination of pathogens on fresh produce.
Charles Sweat, chief operating officer of Natural Selection Foods, announced that his company will require a number of measures be taken by growers that supply their company with the fresh-cut produce that they pack. These measures include working with growers from seed to harvest, inspecting the seed, irrigation water, soil, plant tissues, and wildlife. The company also indicated that sanitation protocols for farm equipment and packaging supplies will be enhanced and monitored, and that a "firewall" will be set up to test all the freshly harvested greens before they enter the production stream.
"Clearly things have to change throughout the leafy greens
industry and the changes need to occur quickly," Farrar says. "We
have relayed to industry that the solution must include specific,
measurable, enforceable on-farm food safety practices that are based
on the best science that's available now."
According to GAP guidelines, areas that should be considered to minimize the potential for microbial contamination of produce include
- agricultural water used for irrigation or crop protection sprays
- wild and domestic animals
- worker health and hygiene
- the production environment, which includes the use of manure, previous land use, and use of adjacent land
- post-harvest water used to wash or cool produce
- sanitation of facilities and equipment.
The FDA instituted a Produce Safety Action Plan in 2004. The action plan builds on previous guidance and addresses microbial food safety hazards and good agricultural and management practices common to growing, harvesting, washing, sorting, packing, and transporting of most fruits and vegetables sold to consumers in an unprocessed or raw (minimally processed) form.
The plan contains four objectives: preventing contamination of
fresh produce with pathogens; minimizing the public health impact
when contamination of fresh produce occurs; improving communications
with producers, preparers, and consumers of fresh produce; and facilitating
and supporting research relevant to fresh produce.
"A significant change is that we've gone from a broader-scope guidance in the past to more commodity specific guidance," says Nega Beru, Ph.D., director of the CFSAN's Office of Plant and Dairy Foods. "Certain commodities account for most of the foodborne outbreaks associated with produce."
As part of the plan, the FDA has provided technical assistance to help industry develop food safety guidance for five commodity groups: cantaloupes, lettuce and leafy greens, tomatoes, green onions, and herbs. The guidelines for cantaloupes, tomatoes, and lettuce have been finalized and are available. With FDA assistance, industry work on guidances for herbs and green onions is ongoing.
In March 2006, the agency released draft guidance for the fresh-cut produce industry. The agency is working to finalize its "Draft Guidance to Minimize Microbial Food Safety Hazards of Fresh-Cut Fruits and Vegetables." The Lettuce Safety Initiative, developed in August 2006, supports the produce safety plan and covers lettuce and other leafy greens, including spinach.
In August 2006, the FDA met with Virginia officials to discuss outbreaks associated with tomatoes produced on the Eastern shore of Virginia. The FDA worked with the Florida Tomato Exchange and the University of Florida's Institute of Food and Agricultural Sciences to arrange a forum, held in November 2006, to discuss improving tomato safety. Also in November 2006, the FDA announced results of an investigation by state and CDC investigators which found that consuming tomatoes in restaurants was the cause of illnesses of Salmonella Typhimurium. Twenty-one states reported 186 cases of illness to the CDC.
"Produce safety is the number one priority in CFSAN right now," Brackett says. "Our role is to serve as a leader in providing direction for industry and to apply the best science-based approaches toward building an even safer food supply. As a result of effective collaboration with our public health partners, the American food supply continues to be among the safest in the world. But we also know that we must continue to work on reducing the incidence of foodborne illness to the lowest level possible."
E. coli Outbreaks at Taco Bell and at Taco John's
On Dec. 14, 2006, the Centers for Disease Control and Prevention (CDC) announced that the Escherichia coli (E. coli) O157:H7 outbreak linked to Taco Bell Restaurants in northeastern states appeared to be over. Based on a number of factors, shredded iceberg lettuce is considered overall to be the single most likely source of the outbreak at this time. The FDA announced that it continues to narrow its investigation by focusing efforts on finding the sources of shredded iceberg lettuce served at the restaurants.
The peak of the outbreak occurred from the last week of November until the beginning of December. A total of 71 cases in five states were reported to the CDC: Delaware (two cases), New Jersey (33 cases), New York (22 cases), Pennsylvania (13 cases), and South Carolina (one case—this person ate at a Taco Bell in Pennsylvania). Fifty-three hospitalizations and eight cases of hemolytic uremic syndrome (HUS) have been reported. HUS can cause permanent kidney damage and death.
FDA investigators reviewed Taco Bell's records in order to trace the distribution channels of the iceberg lettuce and identify the farm or farms where the lettuce was grown, as well as all the firms and facilities that handled the product. This outbreak has been traced to California's Central Valley.
In January 2007, the agency also announced that it had moved closer to identifying the source of illness for an outbreak of E. coli O157:H7 at Taco John's Restaurants in Iowa and Minnesota. The FDA and the state of California, working with state health officials in Minnesota, Iowa, and Wisconsin, have DNA-matched the strain of E. coli O157:H7 bacteria associated with the outbreak with two environmental samples gathered from dairy farms near a lettuce-growing area in California's Central Valley. The outbreak sickened 81 people in November and December 2006. Illnesses were reported in Minnesota (33), Iowa (47), and Wisconsin (one). Twenty-six people were hospitalized, and two suffered from HUS. No deaths have been associated with the outbreak.
Produce Safety Tips
In light of recent contaminated produce outbreaks, the FDA is emphasizing advice to consumers on how to reduce the risk of foodborne illnesses from fresh produce.
- Purchase produce that is not bruised or damaged.
- When selecting fresh-cut produce—such as half a watermelon or bagged mixed salad greens—choose only those items that have been refrigerated or surrounded by ice.
- Bag fresh fruits and vegetables separately from meat, poultry, and seafood products when packing them to take home from the market.
- Strawberries, lettuce, herbs, mushrooms, and other perishable fruits and vegetables can best be maintained by storing in a clean refrigerator at a temperature of 40 degrees F or below. If you're not sure whether an item should be refrigerated to maintain quality, ask your grocer.
- All produce that is purchased pre-cut or peeled should be refrigerated within two hours to maintain both quality and safety.
- Keep refrigerators set at 40 degrees F or below. Use a refrigerator thermometer to check!
- Many pre-cut, bagged produce items like lettuce are pre-washed. If so, it will be stated on the packaging. This pre-washed, bagged produce can be used without further washing.
- As an extra measure of caution, you can wash the produce again just before you use it. Pre-cut or pre-washed produce in open bags should be washed before using.
- Begin with clean hands. Wash your hands for 20 seconds with warm water and soap before and after preparing fresh produce.
- Cut away any damaged or bruised areas on fresh fruits and vegetables before preparing or eating. Produce that looks rotten should be discarded.
- All unpacked fruits and vegetables, as well as those packaged and not marked pre-washed, should be thoroughly washed before eating. This suggestion includes produce grown conventionally or organically at home, or produce that is purchased from a grocery store or farmer's market. Wash fruits and vegetables under running water just before eating, cutting, or cooking.
- Even if you plan to peel the produce before eating, it is still important to wash it first.
- Washing fruits and vegetables with soap or detergent or using commercial produce washes is not recommended.
- Scrub firm produce, such as melons and cucumbers, with a clean produce brush.
- Drying produce with a clean cloth towel or paper towel may further reduce bacteria that may be present.
- Keep fruits and vegetables that will be eaten raw separate from other foods, such as raw meat, poultry, or seafood, and from kitchen utensils used for those products.
- Wash cutting boards, dishes, utensils, and countertops with hot water and soap between the preparation of raw meat, poultry, and seafood products and the preparation of produce that will not be cooked.
- For added protection, kitchen sanitizers can be used on cutting boards and countertops periodically. Try a solution of one teaspoon of chlorine bleach to one quart of water.
- If you use plastic or other nonporous cutting boards, run them through the dishwasher after use.
For More Information
Issues Final Guidance For Safe Production of Fresh-Cut Fruits
(Press Release, March 12, 2007)
- The FDA page on E. coli Outbreaks
- The CDC page on E.coli Outbreaks