The second in a series investigating the complex linkages between human, animal and environmental health: The Infection Loop.
Ashley Armstrong's parents haven't let her eat green salad in five years.
While other parents struggle to get assorted greens into their children's bellies, the Armstrongs have left salad off Ashley's plate since September 2006, when the E. coli from a bag of spinach nearly killed her. Then 2 years old, Ashley was left with just 10 percent kidney function.
"We were totally naive," says her mother, Elizabeth, who now serves on the board of the Center for Foodborne Illness Research and Prevention, a public health advocacy group. "We assumed that the food we bought at our grocery store was safe. We assumed that the FDA, or whomever, had checked to make sure it was safe. We've since found out that's not the case."
Inspectors failed to pinpoint the exact source of the E. coli outbreak that killed three people, sickened 205 and cost the spinach industry $100 million. About a mile from one contaminated spinach field, however, they found a wide range of suspects: high levels of the bacterium in free-range angus cows and their dung, and its genetic match turned up in local feral pigs, soil and surface water.
"There were so many different possible sources that we couldn't say for sure how the spinach got contaminated," Michele Jay-Russell, a food safety specialist at the University of California, Davis, told HuffPost. "But it raised awareness that cattle and wildlife intruding into the field or waterways could be risks for moving pathogens into the produce environment."
As far as Elizabeth Armstrong was concerned, all that mattered was that "somehow poop got in the plant."
It wasn't an isolated incident. Foodborne pathogens strike roughly one in six Americans every year, sickening 48 million, hospitalizing 128,000 and killing 3,000, according to the U.S. Centers for Disease Control and Prevention.
And choosing local and organic options, even going vegan, isn't enough to guarantee safety. Between 1998 and 2007, produce sickened almost 27,000 Americans in the course of nearly 700 foodborne illness outbreaks, according to the Center for Science in the Public Interest. The nonprofit group suggests that produce outbreaks now surpass the number of outbreaks originating in poultry, beef, pork or eggs.
In their wake, these waves of outbreaks helped prompt the U.S. government to implement new regulations, including some standards specific to produce safety.
Contaminated fruits and vegetables tend to be those that grow closest to the ground -- bean sprouts, lettuce and the like -- as evidenced recently by the suspected contamination of California romaine lettuce via manure-laden lagoons and of Oregon strawberries from deer feces.
Now, America's most deadly known foodborne-illness outbreak in more than a quarter-century has added a new danger to the list: cantaloupe contaminated by the bacterial infection listeria. Since the end of July, at least 28 people have been killed and 133 sickened after eating cantaloupe grown at Jensen Farms in southeastern Colorado. (An average produce outbreak can be linked to 39 illnesses, according to the Center for Science in the Public Interest.)
"We have rarely, if ever, seen this pathogen in produce," says Sandra Eskin, director of the food safety campaign with the Pew Charitable Trusts. This outbreak marks the first documented case of listeria in cantaloupe.
Only since the 1990s has produce emerged as an "important vehicle of transmission," says Jay-Russell, noting the heightened attention after the 1996 outbreak of E. coli in Odwalla unpasteurized apple juice.
One of produce's problems is that people tend to eat it raw, and therefore it misses a "kill step" such as heating or cooking. Jay-Russell says that means that oversight has to focus on the entire "food continuum, from the fields to the fork."
In Centennial, Colo., Jeni Exley, her husband and their college-age daughter ate cantaloupe from Jensen Farms with no ill effects. In nearby Littleton, however, Jeni's 84-year-old father, Herb Stevens, was not so lucky.
Before his bout with listeria, Stevens was independent. Since battling the infection, with its attendant fever, muscle aches, diarrhea and other symptoms, he requires daily nursing care and a walker.
Stevens and his wife hadn't worried about their cantaloupes. The elderly couple always bought by the half: not so much that they'd have to throw any leftovers away; cut open to offer a sneak peek inside. But listeria is invisible to the naked eye and easily transferred by knife from the rough, contaminant-inviting surface into the flesh. Once inside, the fruit's low acidity further encourages the bacteria's growth.
According to a federal report released last Wednesday, the Food and Drug Administration, the state of Colorado and Jensen Farms narrowed the listeria outbreak's root cause down to poor sanitation inside a packing facility used by the farm. Tests by the investigators, including experts in agriculture, veterinary medicine and environmental health, ruled out contamination in the farms' fields and irrigation systems, as well as any links to adjacent land use or animal intrusions.
Any of these pathways were reasonably suspect in this case, given listeria's widespread presence in the environment. Research led by Martin Wiedmann, a food science expert at Cornell University, found the pathogen in samples collected throughout New York state -- from sidewalks, parks, ponds, rivers, even the middle of state parks. Another study found that farmers brought listeria home on their clothing and shoes. To a lesser extent, listeria even landed in nonagricultural homes.
The pathogen is persistent, even hardy, withstanding cold temperatures and showing an ability to survive more than a decade indoors. "Bacteria are always trying to be one step ahead of us," says Jay-Russell of UC Davis.
Fortunately, as pervasive and aggressively adaptive as it is, listeria is typically only dangerous on the order of billions of cells, Cornell's Wiedmann said. And only certain subtypes, such as the monocytogenes strain identified on the cantaloupes, repeatedly appear in human outbreaks.
Jensen Farms adhered to safe practices in their melon production operations, such as the use of drip irrigation and plastic mulch to keep cantaloupe from resting directly on the soil, according to Michael Bartolo, a senior research scientist at the Arkansas Valley Research Center in Rocky Ford, Colo. However, there was still plenty of room for contamination.
On Wednesday's media call, Sherry McGarry of the CDC described a few likely culprits in Jensen's packing facility. The building's poor design allowed water to pool on the floor, and the lack of a pre-cooling procedure may likewise have helped incubate bacteria in condensation on melons moving from the warm outdoor air to cold storage.
Of course, that first microbe had to come from somewhere. McGarry suggested that low levels of listeria may have originally been present in the fields and subsequently been carried inside. A truck used to haul culled cantaloupe to a cattle operation was also parked adjacent to the packing facility, suggesting that feces may have hitched a ride.
"The investigation is still open," says McGarry. "There may be details that we are unable to provide at this time."
THE FOUR W'S
A wide range of human and environmental factors can in fact open the door for listeria, E. coli, salmonella and another foodborne pathogens to invade the human body. Eskin points to four general categories that account for most foodborne illness outbreaks: water, waste, wildlife and workers.
Pathogens don't live well on produce that is exposed to the sun and hot temperatures -- unless there's lots of water around.
In the wake of Tropical Storm Irene, Vermont farmers are tossing out perfectly good-looking potatoes and winter squash. The farmers know that if floodwaters come in contact with the edible parts of plants, there is danger of contamination from overflowing septic systems, wastewater treatment plants or soils laden with feces from dogs, deer or cattle. Even planting seeds during or after a flood can be risky.
Those factors are all key to pathogen development and spread, but scientists see one consistent starting point. "It's safe to say that most pathogens that make humans sick begin in the gut of an animal," says Pew's Eskin.
Many animals harbor and deposit microbes that are harmful to humans, but not always to the animal itself, explains Michael Doyle, director of the Center for Food Safety at the University of Georgia. From an animal's intestinal tract, the toxins can travel into feces and then onto an agricultural field through grazing, water irrigation or as fertilizer.
Close proximity between crops and cattle, especially if the grazing cattle are upslope of a field, may be particularly dangerous for produce. In 1985, the first reported outbreak connecting listeriosis to food was traced back to sheep that grazed in the vicinity of a cabbage field harvested for coleslaw.
Wild animals poop, too. "We don't grow food in a sterile environment or in a bubble. It's outside in the dirt," says Jeffrey LeJeune, a professor of food science, environmental and animal health at The Ohio State University. "If a bird flies overhead and decides that it's had enough to eat, it could leave a deposit on a melon or a tomato."
Fences can be helpful, but such restrictions on wildlife movement are controversial among ecologists. Jay-Russell suggests other approaches that have been adopted by many California growers, such as avoiding planting where there is a major wildlife corridor and walking the fields before harvest.
Other species aren't always responsible for contamination. Human waste, a likely contributor to this year's bean sprout E. coli outbreak in Germany, is also a consistent threat to the food supply. Produce can be at risk if a single worker doesn't wash his or her hands thoroughly.
"How many people touch a cantaloupe between the farm and table? A whole lot more than the number of armadillos that do," LeJeune says. "If we could solve all the problems of all of the animals, the problem wouldn't go away."
RECALLS PROMPT REGULATION
The government recently caught on to the fact that investing in prevention could pay off in terms of both lives and money saved. A 2010 report published by the Produce Safety Project at Georgetown University estimates that foodborne illness linked to produce costs the United States almost $39 billion a year.
"In the last three or four years, the CDC and health departments have picked up outbreaks that five years earlier would have never been detected," says Doyle.
They are also detecting the outbreaks more quickly, thanks in part to increasingly sophisticated DNA fingerprinting tools. In the case of the listeria-contaminated cantaloupe, agencies came together with a "quick and effective response," says FDA commissioner Margaret Hamburg during a media briefing last Wednesday.
Yet many experts say the real measure of progress is not the ability to detect outbreaks, but to prevent them in the first place.
In January, President Barack Obama signed into law the Food Safety Modernization Act, which establishes regulatory standards for the safe growing, harvesting, sorting, packing and storage of fresh fruits and vegetables. FSMA takes into account both manmade and naturally occurring hazards, and includes requirements to ensure the safe import of food from foreign facilities.
In effect, the new law reverses the orientation of FDA's food safety activities from reaction to prevention. "That's huge," says Eskin. "By starting at the beginning of the food chain rather than the end, hopefully they'll need to do less responding down the road."
For example, the law will require inspectors to make regular visits to fields like Jensen Farms to identify sources of contamination before it has an opportunity to make anyone ill -- similar to regular restaurant inspections. It will also create the first-ever mandatory national safety standards for produce.
"Lessons from [the listeria] outbreak speak to the urgency we have in implementing the FDA's Food Safety Modernization Act, which gives FDA much-needed tools to build a new prevention-focused food safety system," said Hamburg. Since 1998, the FDA and USDA have issued guidance on "Good Agricultural Practices" for producers to follow, but such urgings have no enforcement behind them.
As they finalize the new food safety laws, Jay-Russell says federal regulators should draw inspiration from the Leafy Green Marketing Agreement, which California and Arizona put in place after the 2006 spinach E. coli outbreak. Experts from the two states, which produce 90 percent of the country's leafy greens, developed a wide range of food safety metrics, from how often to test irrigation water to the optimal method of composting and proper use of animal manures. Further, leafy green growers generally plant and grow in Northern California between late spring and fall, and then move on to southern California and Arizona for the winter to avoid floodwaters.
Despite its promise, some experts still have concerns over the new federal regulations. The FSMA exempts small farms, where contamination can easily go unnoticed.
"I'd love to say that if you grow food in your backyard and raise your own cows, you'd be safe. But that's not the way it is. Both small and large producers have to take precautions to keep feces out of our food," says Bill Marler, a lawyer who made his name as the "E. coli guy" representing victims of the infamous Jack in the Box outbreak in the early 1990s. He now represents dozens of victims and families affected by the listeria outbreak.
The outbreaks that make the news tend to be the big ones, and usually associated with large producers. "It's easier to pinpoint an outbreak when it poisons hundreds of people," Marler says.
United Fresh Produce Association spokesman Ray Gilmer says he agrees that "small farms shouldn't get a pass on food safety." Other than their opposition to this exemption, the lobbying group, which represents farmers, grocers and restaurant chains, is all for beefed up regulations. Gilmer said, "The produce industry came to the cumulative realization several years ago that it is in everyone's best interest to pass a new law and ensure consistently high enforcement of the best possible food safety standards."
As long as the new rules for production practices are "scientifically valid", he suggests there isn't anything they wouldn't be willing to do.
Lack of funding is also a threat to FSMA implementation. The House recently voted to cut 2012 funds for the FDA's food safety program, despite the agency's request for a raise to cover increased costs for improved technologies and more inspections, up to once every three years for facilities deemed high-risk.
The FDA only inspected about 15 percent of U.S. food production facilities in 2010. Before this year's outbreak, Jensen Farms had never hosted a federal inspector.
Eskin tells HuffPost that Pew advocated for "higher minimum frequencies for facility inspections." Still, she says, there is no "magic number."
"We have seen outbreaks at plants that were consistently inspected," adds Wiedmann.
Wiedmann suggests that it is most vital to invest in research, technology and tools to help producers develop safe systems. "If the government has the ability to quickly and effectively detect an outbreak and trace it back, then companies know that if they do something wrong, they will get caught," he says.
"The hard truth," says Wiedmann, "is that 100 percent safe food is virtually impossible as long as we grow food exposed to the environment."
LAST LINE OF DEFENSE
No matter how rigorous or enforceable the regulations, experts caution that some factors will always remain out of the government's control.
Food safety education for consumers, including proper hand and produce washing, "cannot be overemphasized," says Bruce Kaplan, a retired veterinarian in Florida and advocate for One Health, a movement that recognizes the interconnectedness of human, animal and environmental health.
Keeping animals healthy is also key. "It's a very small world and we're all interconnected in it," says Eileen Choffnes, a scholar and director of the Institute of Medicine's Forum On Microbial Threats. This December, the forum is slated to host a meeting on One Health's ability to improve food safety.
Vaccinating cattle against infection could help, according to Thomas Besser, a professor of microbiology in the Food and Waterborne Disease Research Program at Washington State University's College of Veterinary Medicine. So can simply providing them with contaminant-free food and water.
Unfortunately, developing an effective vaccine and providing cattle with "microbiologically clean water" are proving to be difficult tasks, Besser says, given how easily food and feces can contaminate an animal's drinking source. He is currently looking into alternative watering systems that go beyond the bucket, such as training animals to drink out of a hose or press a lever to get water.
Another lingering mystery is the apparent seasonality of microbes in some animals. Cattle in particular have been found to shed more pathogens during the summer and fall, notes Jay-Russell. E. coli nearly disappears in the winter.
"This seasonal variation is a big question," says Besser. "If we can find out what causes the summertime increase, and depending on what that is, we might be able to reduce the number of cattle infected by 90 percent."
Research into animal biology could help identify new strategies to prevent or treat listeria as well. Unlike other pathogens such as E. coli, listeria can sicken both humans and animals, explains Jay-Russell. Because sheep, goats and cattle develop similar symptoms to humans, she suggests studies of this parallel animal disease could lead to a better understanding of human illness.
A One Health perspective is useful in solving such puzzles, suggests Kaplan.
"Had One Health principles been implemented 50 years ago, there would be many people who would not have suffered, not have died needlessly as they continue to do," he says.
The latest deaths linked to the listeria outbreak from tainted cantaloupes were reported on Tuesday. It is "too soon to declare the cantaloupe outbreak over," given the long incubation period of the pathogen, Barbara Mann of the CDC said during last Wednesday's media briefing. Plus, there appears to be a steady stream of outbreaks to take its place.
"It seems that every couple of months, there is yet another foodborne outbreak, and it usually has a fairly large footprint, either in terms of the number of people sickened or the geographic range of product distribution," says Choffnes. "Even a single event can have a very large impact on not only human and animal health, but the economy."
Shortly after the cantaloupe recall came announcement of a listeria-based recall of chopped romaine, caught early thanks to a newly launched federal research effort to gauge food-safety conditions surrounding leafy green vegetables. And late last week, another sample test by the FDA uncovered contamination in bagged spinach, resulting in another preemptive recall.
"Food is not as safe as we think it is," Elizabeth Armstrong says. Shopping at a grocery store for her family, she says, is now "an act of faith."
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