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Consumer Reports: Leafy greens safety guide

In an age of rampant romaine contamination, can our salads be saved?

When Carolyn Graham ordered a garden salad at a pizza restaurant near her hometown of Loomis, Calif., on a weekday night in April 2018, she felt good about what she thought was a healthy choice.

But by the weekend, she had stomach cramps and diarrhea, which grew more severe with each passing hour. By 11 p.m. that Saturday, the diarrhea had turned bloody, and it continued all night long. Around 6 a.m. Sunday, she and her husband, Kenneth, headed to the emergency room. Doctors gave her fluids, oxygen, and an antibiotic, but Graham’s symptoms didn’t abate.

It took doctors three days of testing and analyzing results to determine that Graham had been infected with E. coli O157:H7, a dangerous strain of the bacteria that produce a substance called Shiga toxin. Graham, who was 72 and had been in excellent health, had developed a form of kidney failure called hemolytic uremic syndrome -- a side effect that occurs in 5% to 10% of people who contract O157:H7.

Doctors put Graham on dialysis to help her kidneys function properly again, but she was going in and out of consciousness during her 14-day hospital stay. Her husband, one of her daughters, and a granddaughter stayed by her bedside until she was fully conscious and able to recognize the people around her. Then, her husband says, “she had to relearn how to talk, how to walk,” a rehab process that took about two months before she was back to normal.

The culprit in Graham’s ordeal? The romaine lettuce in that seemingly innocuous garden salad. That spring, the Centers for Disease Control and Prevention and the Food and Drug Administration sent out multiple national alerts, eventually telling people not to eat romaine from the Yuma, Ariz., area. Graham, it turned out, was one of 240 people across 37 states in the U.S. that spring who government officials say became sick from tainted romaine. It was the largest national E. coli O157:H7 outbreak in more than 20 years: Almost half of those affected were hospitalized, and five people from four states died. Then, right before Thanksgiving that same year, supermarkets and restaurants pulled romaine from their shelves and menus after federal officials announced yet another E. coli outbreak.

The Return of Outbreaks

Just as consumers thought perhaps the 2018 E. coli outbreaks were a distant traumatic memory, romaine-related illnesses returned. In outbreaks starting in October 2019 and continuing into December, 133 people were sickened. This was despite steps taken over the past two years by farmers and the FDA to identify the sources of the outbreaks.

Consumer Reports is actively advocating for improved inspection and farming practices to better protect the lettuce food supply. At CR, we are also surveying Americans about their habits and working to debunk myths, including the perception that “triple washed” packaged lettuce is always safe -- when, in fact, the washing process doesn’t remove all harmful bacteria.

“It’s astonishing how frequently the lettuce-consuming public has been exposed to bacteria like E. coli over the years,” says Bill Marler, a food safety lawyer in Seattle who negotiated a settlement for Graham. “I have dozens of clients [over the years] whose lives have been completely upended,” he says. “They’ve needed kidney transplants and had hundreds of thousands of dollars in medical expenses because they chose to eat a presumably healthy food.”

In fact, between 2006 and 2019, romaine and other leafy greens, such as spinach and bags of spring mix, have been involved in at least 46 multistate E. coli outbreaks, according to the CDC. Some research shows that greens cause more cases of food poisoning than any other food, including beef.

The constant drumbeat of romaine-related E. coli outbreaks has made Americans very worried about eating lettuce. In a 2019 nationally representative Consumer Reports survey of 1,003 Americans, 52 percent admitted being concerned about getting sick from leafy greens -- more than those who are worried about poisonings from beef, chicken, or eggs. Sales of romaine, which was until recently the most popular lettuce in the U.S., are down in the wake of the 2018 outbreaks, dropping about $98 million to $465 million from their $563 million peak in 2017, according to data from market research firm Nielsen. (Iceberg has regained the No. 1 spot.) Meanwhile, lettuce growers and the FDA have been trying to figure out where -- from farm to fork -- the potentially deadly bacteria are finding their way into and onto lettuce leaves.

Frank Yiannas, deputy commissioner for food policy and response at the FDA and the agency’s top food official, told CR: “FDA has been working tirelessly to prevent these [outbreaks]. But we’re going to work harder. It’s a high priority for the agency and a high priority for me personally.”

In the meantime, for those who want to continue to get the health benefits of leafy greens, there are safety guidelines that can help to mitigate the risk. (See “The Safest Ways to Eat Salad.”)

Salad Under Siege

How did leafy greens -- nutrient-packed foods recommended by doctors and nutritionists alike -- become so risky? And why is romaine linked to so many of these outbreaks?

It comes down to the modern way we grow, harvest, and package our salad greens. “There are many opportunities along the continuum-- from seed all the way to a consumer’s plate­ -- for greens to become contaminated,” says Ben Chapman, Ph.D., a professor and food safety extension specialist at North Carolina State University in Raleigh.

Part of the reason greens in particular are so problematic is the sheer volume we’re consuming. The leafy greens industry ships about 130 million servings per day all year long -- enough to supply a daily salad fix to nearly 40 percent of Americans. And almost a quarter of the greens being consumed are romaine lettuce.

Perhaps most important: Salad greens are almost always eaten raw, unlike burgers, eggs, flour, and many other foods that can be contaminated with pathogens but are usually cooked enough to kill any bacteria. “You can destroy E. coli and other bacteria with enough heat, but few people are going to cook their lettuce,” says James E. Rogers, Ph.D., director of food safety research and testing at Consumer Reports.

“A food that doesn’t have a final consumer ‘kill step’ presents some extra challenges [for] food safety,” says Matthew Wise, Ph.D., deputy chief of the CDC’s outbreak response and prevention branch. “That’s probably the main driver” among a number of factors that can cause an outbreak, he says.

“We face a real dilemma with leafy greens, especially romaine lettuce,” says Rogers. “They’re packed with nutrients, so we don’t want to discourage people from eating them. But we can’t ignore the fact that leafy greens are potentially risky, perhaps one of the riskiest foods.”

But, he says, we need answers on what’s happening with greens sooner rather than later. “More needs to be done to determine the exact sources of contamination with dangerous bacteria,” he says. “Once that’s done, the FDA must set strict requirements for growers and processors, which will help prevent people from getting sick.”

While the odds that you’ll get sick from eating any single salad are low, Rogers says, they’re real. “When you hear about 100 or 200 people contracting a foodborne illness, it may not sound like that many, but for every case of food poisoning that’s reported, there are many, many more cases that never get reported.” In fact, according to the CDC, for every reported case of E. coli O157:H7 infection, there are probably 26 that have gone undocumented.

Listeria in Leafy Greens

Leafy greens can be the source of other bacteria that can make you sick, too. As the chart below shows, greens have been involved in outbreaks of salmonella, campylobacter, and Listeria monocytogenes in addition to E. coli.

To check for the presence of harmful bacteria, CR’s food safety scientists tested 283 samples of bagged and whole heads of six types of leafy greens, including romaine, spinach, and kale, plus mixes of greens in the spring of 2019.

While we didn’t find the dangerous E. coli O157:H7 implicated in recent romaine lettuce outbreaks, we did find that certain samples contained coliform bacteria. “This type of bacteria doesn’t make people sick, but it’s a sign that feces may have come into contact with the lettuce, and when we see it, it’s considered a harbinger of possible contamination with harmful bacteria,” says CR's Rogers. There was no difference in bacteria levels between whole head and packaged greens; packaged greens that were labeled “triple washed” had bacteria levels similar to those in packages marked “unwashed.”

More worrisome: We also found Listeria monocytogenes—dangerous bacteria found in the environment, especially in the cold, moist conditions of refrigerators and food-processing facilities—in six of the samples: two bagged and four loose heads. CR immediately informed the FDA, the CDC, and the companies. One of the samples had a strain genetically linked to at least two cases of listeriosis (the illness caused by listeria) reported to the CDC. Listeriosis is rare, but it kills about 20 percent of those affected, compared with less than 1 percent for E. coli, campylobacter, and salmonella. (See “Leafy Greens With Listeria Sold at Major Supermarkets.”)

From Farm to Table

So how do bacteria get into the greens in the first place? To answer that, it helps to understand the critical water needs of greens and how they are sometimes grown near livestock -- both of which can open a pathway to contamination. John Boelts, a farmer in Yuma, owns one of the 60-plus farms that cover a stretch of land from Yuma and the surrounding area to California’s Imperial Valley. That’s where the vast majority of leafy greens on the market in the U.S. and Canada are harvested in winter. The Yuma growing season begins with the planting of seeds in August in the hot, arid desert. Over the next few months, the dusty brown fields become filled with rows of emerald green heads of romaine, iceberg lettuce, vegetables, and fruits. Harvesting begins in late October.

Lettuce grows best when daytime temperatures are moderate and nights are cool, so as the weather in the Yuma region warms up, lettuce production shifts to California, moving in seasonal increments throughout the Southern Coast, Central Coast, Salinas Valley, and parts of the Central Valley. Although the soil and environment differ in all these regions (including Yuma), one thing they have in common is that they don’t get much rain—and greens need a lot of water to grow (as much as 36 inches per acre), so all those lettuce fields require irrigation. At farms around Yuma, such as Boelts’, water is channeled from the nearby Colorado River through a system of irrigation canals.

Once the greens grow to maturity, they’re harvested, mostly by hand, Boelts says. Growers take samples of the greens to check for harmful bacteria (but they don’t check every leaf, which is why the bacteria sometimes slip through). Some greens are packed right in the field, to be immediately cooled and shipped to stores. Greens that are destined to be bagged or sold in plastic containers -- 65% of Americans buy packaged greens, according to market research firm Mintel—are taken from the field to processing plants, where tons of lettuce from multiple farms are mixed together. (Romaine is produced to the tune of 1.5 million tons per year.) There, the lettuce is usually washed in water that contains chlorine or another sanitizer, then rinsed, dried, packaged, and shipped to supermarkets and restaurants across the country.

Contamination From Cattle

What any lettuce farmer will tell you is that he or she fears the animals that live around lettuce fields. That’s because E. coli O157:H7 and other strains of illness-causing bacteria live in the guts of cattle and other animals, including sheep, deer, wild boar, and even birds. Although the E. coli bacteria don’t usually make the animals sick, when they defecate they deposit dangerous bacteria into the soil and water around them. That contaminated soil could later end up mixed with dirt tracked by equipment, people, or animals onto a field full of leafy greens, or rain could wash the bacteria into one of the open irrigation canals that are so important for lettuce-growing regions.

This route to food poisoning has been known about for longer than a decade: In 2006, in an E. coli O157:H7 outbreak linked to spinach, federal officials said that a possible source was waste from feral pigs that got into growing fields.

Because animals can contaminate their valuable crops, farmers put a lot of effort into keeping them away. “We pay people to stand by fields and scare birds off,” Boelts says. “We surround fields with 8-foot-tall fences, prohibiting animals from being on our farm. We’re doing everything science says we should,” he says.

But contamination still occurs, and experts and research say it’s because fields of leafy greens are sometimes located next door to large cattle farms known as concentrated animal feeding operations (CAFOs).

“It’s because of the proximity of cattle feedlots to fresh produce fields,” says Keith Warriner, Ph.D., a professor in the department of food science at the University of Guelph in Ontario who has studied foodborne illness linked to produce. “In the Salinas Valley, you’ll see cattle roaming the hills.” (Romaine from the Salinas region was linked to the outbreaks in fall 2018 and fall 2019.) “With every outbreak, there’s a cow somewhere,” says attorney Marler, who has tracked food-poisoning incidents linked to greens for almost 20 years.

It has also been suspected that bacteria mix with the soil and become part of the dust, which can be carried by the wind from a CAFO and deposited onto the greens as they grow in the field. But experts and investigators from the FDA and CDC have focused on contaminated irrigation water as the most likely vector. “E. coli-tainted manure can run off down hills and into rivers, contaminating water sources,” Warriner says.

An FDA investigation to identify the source of the contamination in the spring 2018 outbreak that sickened Carolyn Graham never reached a firm conclusion. But investigators strongly suspect an irrigation canal that reportedly provided water to the 36 romaine fields involved in the outbreak. They found the E. coli outbreak strain in three samples taken from the canal, which is next to a CAFO that houses more than 100,000 cows.

The source of the Thanksgiving 2018 outbreak is also still a mystery, but the FDA did find the strain of E. coli that made people sick in sediment from a water reservoir on one of the California farms that grew contaminated lettuce. It’s possible that droppings from wild animals tainted the water, but there is also a CAFO near the lettuce farm.

“These findings suggest that to solve the lettuce problem, we really have to solve the cow problem,” says Michael Hansen, Ph.D., senior scientist at Consumer Reports. “Yet even though nearby CAFOs were thought to be the source of the bacteria that caused the outbreaks, under the law the FDA wasn’t allowed to access those feedlots, and that dead-ended the investigation.”

The Riddle of Romaine

The science doesn’t clearly show that any leafy green is more or less risky than another, but some researchers suspect that romaine may be particularly vulnerable to contamination because its leaves are so delicate.

“It can get damaged easily, which makes it easier for the bacteria to get into it,” Warriner says. In fact, when the romaine involved in the Yuma outbreak was growing in the fields, the weather turned cold and windy, possibly injuring the leaves. Although other greens have been involved in outbreaks, Warriner says, “some, like kale and spinach, are tougher, and they’re high in natural antimicrobial compounds called thiocyanates. These greens were irrigated with the same water as the romaine involved in the Yuma Valley outbreak of 2018, but they weren’t affected.” Also, while other greens are susceptible for these same reasons, they aren’t produced in the same quantity, so they’re less likely to cause a major outbreak.

Then there’s the math: We simply eat a lot more romaine than other dark leafy greens. “Romaine lettuce remains beloved in the U.S.,” says Kara Nielsen, a food trend expert in Oakland, Calif. Despite drop-offs in sales, it’s the second most popular salad green. And it’s everywhere: Romaine serves as the base for Caesar salads and is often in sandwiches, wraps, and burritos. And it’s challenging to find a package of mixed greens that doesn’t contain romaine.

Problematic Packaging

Certain labels proclaim that the greens have been triple-washed. Will that protect you from getting sick? Not necessarily.

When bacteria such as E. coli come into contact with any type of lettuce, they’re almost impossible to wash off completely, according to the CDC and other researchers. That’s in part because disease-causing bacteria can get inside the leaves of the greens as they’re growing, when contaminated water taken up by the roots is dispersed throughout the plant. What’s more, surface bacteria can adhere stubbornly in the wrinkles and grooves in the leaves. “The purpose of washing greens -- in the field or at a processing facility -- is simply to remove dirt and grit, not bacteria,” says CR’s Rogers. According to CR’s own recent lettuce tests, washed and bagged lettuce isn’t any cleaner, bacteria-wise, than whole heads of lettuce.

Although the washing process for packaged greens can remove up to 99 percent of bacteria as it’s removing dirt and grit, food safety expert Chapman says even the small amount that remains may make you sick. “Shiga-toxin-producing E. coli has a very low infectious dose -- as little as 10 microscopic cells are all it takes, according to some estimates,” says Rogers.

And greens destined for packaging carry unique risks: “A bag or box of greens often contains leaves from many different farms that have been mixed together at the processing plant,” says CR’s Hansen. And because the leaves may be cut or shredded, the bacteria have more entry points. “So if there is even a small amount of bacteria-carrying lettuce in the batch, from just one farm, it can contaminate many, many packages of greens,” he says. In fact, in the 2006 spinach outbreak, the tainted greens were eventually traced to one small section of just one grower’s field. In addition, cut or damaged leaves secrete juices that feed bacteria, if they are present, and the juices can collect in the packages.

A Need for More Inspections

The challenge, then, is figuring out which steps will decrease the risk of contracting food poisoning, says Rogers. He says making salads safer will require close attention by growers and regulators at every step of leafy green production. “Unless something changes in the way greens are grown and processed, outbreaks will continue to happen,” he says.

People within the industry are making ongoing efforts to improve the situation. “We are doing everything we can as an industry,” says Scott Horsfall, CEO of the California Leafy Greens Marketing Agreement. “It’s a very important and efficient system for the most part, but we are very focused on eliminating the illnesses that do occur.” Upwards of 97 percent of leafy greens growers in Arizona and California now follow the standards set by the LGMA, which include mandatory inspections to ensure that they’re following standards -- though the results of these audits are not public.

LGMA standards put in place by the Arizona and California LGMAs after 2018 require that if surface water is going to be used for overhead irrigation, where it would touch the greens' leaves, in the 21 days before harvest, it needs to be tested at least once and treated. The minimum buffer zone between CAFOs and fields of leafy greens was tripled, from 400 feet to 1,200 feet, based on research indicating that E. coli could travel 600 feet, and fields in California must be at least a mile from larger CAFOs.

Some growers, like Boelts, say they’ve gone even further, ensuring that no irrigation water touches edible portions of any plant and not planting within 2 miles of animal farms. But even these additional safeguards might not be sufficient, according to experts such as Warriner at the University of Guelph.

The FDA, the leafy greens industry, and researchers at the University of Arizona Cooperative Extension are conducting a multiyear study to better understand all the ways that produce may become contaminated. “We’re collecting thousands of samples over the course of a few years -- soil samples, water samples, air samples, animal footprints -- to see if it can further inform what we know about how contamination might occur, and we’re hopeful that it will,” says the FDA’s Yiannas.

But we may never get to a place where lettuce is considered a low-risk food. Producers have already made most of the changes that we know would improve food safety, so the next steps are going to be harder to uncover, according to Channah Rock, Ph.D., one researcher on the project. “There’s no such thing as zero risk,” she says.

Getting to the Root Source

“We know it’s a complicated problem,” says CR’s Rogers. “But this system is broken, and there are things that could be done that aren’t being done.”

Although members of the LGMA test and now treat surface water that touches edible parts of plants at least once in the 21 days before each harvest, according to the organization’s standards, CR thinks more testing is needed. “The FDA needs to implement the stricter water testing rules that were laid out in the Food Safety Modernization Act,” says CR’s Hansen. Those rules, which require more testing of more water samples, were supposed to take effect in 2018, but they have yet to be implemented and are now pushed out to at least 2022. “The delay is unacceptable,” he says.

And under the FSMA, the FDA is supposed to issue a list of high-risk foods -- defined as those that are often involved in food-poisoning outbreaks or produced in a way that makes them more likely to contain dangerous bacteria -- but has not yet done so. “The FDA should immediately develop this list and put leafy greens on it,” Rogers says. “By law, once a food is deemed ‘high risk,’ the FDA has more authority to require record-keeping and compel recalls,” he says. “That will go a long way toward preventing and controlling foodborne illness.”

CR experts also say that Congress should pass legislation recently proposed by Sen. Kirsten Gillibrand, D-N.Y., and Rep. Rosa L. DeLauro, D-Conn., that aims to strengthen the FDA’s ability to pinpoint the origin of foodborne-illness outbreaks in greens and other produce. The legislation, if passed, would do this by giving the FDA the power to inspect CAFOs to look for the bacteria that could be infecting the lettuce -- something it’s not legally able to do right now.

Being able to trace the origin of the dangerous bacteria is key to halting foodborne outbreaks, says CR’s Rogers. After the 2018 outbreaks, the FDA requested that romaine lettuce producers voluntarily list the region of origin on their packages—and many did. The theory is that if lettuce is labeled and an outbreak occurs, retailers will know exactly what to pull from store shelves and consumers will be able to check labels before buying or eating greens. This kind of labeling is a step in the right direction and should be made mandatory, Rogers says, but “it relies on the shopper knowing first that there’s been an outbreak, and then remembering which part of the U.S. is involved, and then checking the label for information. That’s a lot to ask of consumers.”

People also need to be alerted to food-poisoning outbreaks and recalls more quickly, Rogers says. When the FDA knew of a possible outbreak of E. coli linked to romaine in September 2019, the agency waited six weeks after beginning its investigation before revealing to the public that there was a problem. “I think it’s immoral not to tell the public about contamination as soon as it’s known,” says food safety attorney Marler. “It undermines the public health agencies’ credibility.”

Why the delay? The FDA says that by the time they were made aware of the outbreak, the lettuce was past its expiration date and was no longer on store shelves, so it believed there would be no new illnesses. But, says CR’s Hansen, “Given the continuing problems with romaine, and the seriousness of O157:H7, the FDA should have made an announcement sooner and let consumers decide for themselves if they wanted to continue to eat romaine.”

Editor’s Note: This article also appeared in the March 2020 issue of Consumer Reports magazine.