Safer Salads

Jorge M Fonseca & Sadhana Ravishankar. American Scientist. Volume 95, Issue 6. Nov/Dec 2007.

A s children, we played in the dirt, ate fruit without washing it, licked the juice from our grubby fingers and never fell sick, if memory serves. This last detail probably isn’t quite true, but it’s also possible that something has changed since we were kids-something in the food itself, or in society, that makes us more vulnerable than before. It certainly seems that we hear more frequent reports of people getting sick after eating fresh fruits and vegetables. Why is this? Is it just the press coverage?

Actually, no. It is indeed true that, for fresh produce, the number of outbreaks of food poisoning caused by microorganisms has risen in recent years. There are many potential explanations for this trend. Perhaps most significantly, people are eating more fresh fruits, vegetables and salads than ever before, and more meals are eaten outside the home at restaurants or public gatherings-the most common settings for contracting foodborne illnesses. The greater risk stems partly from centralized preparation and distribution, which can spread contamination over a large volume of food, and partly from the greater number of people in contact with the food-meaning more chances for poor handling and storage. In addition, more of today’s produce is imported from abroad, where standards may be less strict, and transit times from field to table can be longer. Local and national surveillance systems do a better job today than they once did of reporting consumer illnesses. Also, some scientists believe that the proliferation of antimicrobials and antibiotics is partly to blame: Pathogenic bacteria are more likely to grow quickly when they do not have to compete with benign microbes for resources. Several studies have shown an inverse relation between populations of natural microflora and pathogenic bacteria in soil, produce and surfaces in general.

Of Pathogens and Produce

For packaged sprouts during the period from 1995 to 1999, and for leafy greens in more recent years, outbreaks of two bacteria, Salmonella and Escherichia coli O157:H7, have marked these items as particularly vulnerable to becoming vehicles for outbreaks. In the late 1990s, the sprout industry saw several undesirable records made and broken in outbreaks per year and cases per outbreak. According to the Centers for Disease Control and Prevention, during the 24-year period between 1973 and 1997, 32 states reported 190 produce-related outbreaks, which together involved 16,058 illnesses, 598 hospitalizations and eight deaths. More recent data from the Center for Science in the Public Interest show that in the 14 years between 1990 and 2004, produce was implicated in 639 outbreaks involving 28,315 cases-more than a threefold increase in almost half the time.

Among foodborne pathogens, SaImonella bacteria are the prime cause of outbreaks in fresh produce, causing one out of five such outbreaks between 1990 and 2003. The biggest culprits were tomatoes, melons and sprouts. Salmonella is acid-tolerant, which allows it to survive in fruits and vegetables with a low pH, such as tomatoes. Like many of the pathogens that can contaminate produce, Salmonella is an intestinal, or enteric, microbe. Animals shed the bacteria in their feces, and soil that contains fresh or incompletely composted manure from wild or domesticated animals can act as a reservoir for the bacteria. If produce that is grown in contaminated soil is not washed thoroughly, Salmonella on the surface can spread to the inside portion during slicing or cutting. In the case of sprouts, which are not usually sliced, bacteria probably enter the seeds before germination. The situation is complicated by the fact that consumers rarely cook and seldom wash sprouts.

Escherichia coli O157:H7 is a deadly strain of a bacterium that is normally found in all human intestines. As recently as fall 2006, a multistate outbreak linked to bagged spinach killed three people and sickened more than 200. This pathogen was once associated primarily with raw ground beef and undercooked hamburgers but now affects fresh produce, too. The rise in E. coli-tainted fruits and vegetables probably comes from cattle operations, which can contaminate fields through feces or feces-laced irrigation water. Cross-contamination between meat and fresh produce can also take place during processing or packaging, and contact with raw beef is suspected to have been at the root of outbreaks in cantaloupes, sprouts, lettuce and fruit salad in the 1990s. Nearly twothirds of the outbreaks associated with E. coli-contaminated produce have occurred during late summer and fall, when warm temperatures and outdoor cooking can subvert good hygiene, and about half of the outbreaks have involved cross-contamination during food preparation.

Scientists aren’t sure why this strain of E. coli has become so prevalent. Some investigators hypothesize that the type of food that cattle eat determines the quantity and acid resistance of the E. coli O157:H7 bacteria shed in their feces. However, the evidence to support this claim is inconclusive. One study reports that animals fed grain have larger populations of acid-resistant bacteria in their gut compared with animals fed hay. This finding makes sense, because cows lack the enzyme that breaks down starch, leaving it to ferment and acidify the rumen-conditions that create both food and ideal housing for acid-tolerant bacteria. Such bacteria, when shed in the environment, would be hardier than their nonresistant counterparts. If this dietary difference were true, then bacteria from grain-fed cattle would die more slowly in the environment or in the acidic conditions of a human stomach, presenting a greater risk to consumers. However, another study by different investigators found that E. coli O157:H7 shed from cows fed grain was no more acid-resistant than that shed from cows fed hay. The same report indicated that animals fed hay shed the microbe for longer periods than those fed grain. There is no clear epidemiological evidence correlating the presence of E. coli O157:H7 in animals with their diet.

Listeria monocytogenes is a foodborne pathogen commonly found in raw vegetation. The bacterium is ubiquitous and hardy in the environment, able to withstand refrigeration and even grow in such cold, dry conditions. Although fewer people get sick from Listeria than from many other microbes, this pathogen kills its victims more often than any other. In 1981, contaminated coleslaw killed 17 people and sickened 41; the source of the outbreak was believed to be manure from sheep that had listeriosis. In the same decade, this bacterium was a major problem in cheese and dairy products, leading industry regulators to adopt a “zerotolerance policy” in ready-to-eat foods. Since then, stringent control measures have reduced the number of Listeria outbreaks significantly.

Although Salmonella, E. coli and Listeria get much of the attention, many other bacterial pathogens cause outbreaks too, including certain species of Bacillus, Campylobacter, Clostridium, Shigella, Staphylococcus, Vibrio and Yersinia. All are enteric pathogens, and all, with the exception of Shigella, taint fresh produce, most often because of crosscontamination with raw meat or eggs. In recent decades, these bacteria have caused outbreaks traced to many different fruits and vegetables, including cabbage, garlic (chopped, in oil), green onions, lettuce, mixed vegetables, parsley, sprouts, strawberries and watermelon.

Viruses also cause many outbreaks of produce-related foodborne illness, although the contamination is usually through an infected food handler. These viruses require a host and are usually too fragile to survive in the soil or on the produce itself for long periods of time.

Parasitic protozoans (single-celled animals) also account for some produce-related outbreaks. The most common culprit is Cydospora cayetanensis, which hitched a ride to U.S. and Canadian grocery-store shelves aboard Guatemalan berries in the late 1990s. Other protozoan contaminants in recent years have included Cryptosporidium parvum and Giardia lamblia. These parasites infect fruits and vegetables through contaminated irrigation or wash water, causing profuse diarrhea in affected patients. In general, the quality of produce grown outside the United States is monitored by third-party agencies in the foreign country. Very little of the product is analyzed at the U.S. port of entry.

Before the Harvest

The microbes found naturally on produce are very diverse, even between lots of the same crop. In most cases, the microflora that inhabit a fruit or vegetable are similar in the field and after harvest-a fact that highlights the importance of preharvest events on food safety. Fields that are used to contain animals are more likely than other places to harbor enteric pathogens in the soil; in rare cases, pathogenic bacteria can survive for months after the animals are gone. Thus, the U.S. Environmental Protection Agency mandates a minimum waiting period of almost a year after animal husbandry operations cease before growers can cultivate the same field for edible fresh crops. For the same reason, raw manure is a dangerous soil additive for croplands and should be adequately composted (with sufficiently high temperatures) before use as a fertilizer for food crops. (The use of fresh sheep manure caused the major outbreak of Listeria in cole slaw in the 1980s.) Flooded croplands are a particular concern because of their potential to carry bacteria from animal waste into the roots of some kinds of plants.

The type of irrigation system and the quality of the irrigation water directly affect the microbial quality of produce at harvest. Because bacteria contaminate a crop most easily through leaves or fruits (especially damaged areas), it is especially important to avoid irrigation with tainted water. Furthermore, the risk of contamination is higher in produce from fields with an overhead sprinkler system, or in circumstances when the crop is harvested immediately after irrigation or rainfall. In this case, the splashing can carry contaminants from the soil onto the leaves.

Given the risk of having animal feces in contact with food crops, one might think that organically grown crops-which use organic fertilizers such as composted manure instead of synthetic fertilizers-would be especially likely to be contaminated with enteric pathogens. However, this hypothesis appears to be untrue: No clear differences exist between organically grown and conventional produce in terms of microbial safety. It is important to note that such findings apply only to certified organic produce-several studies have shown that noncertified products claiming to be organic (or nature friendly) actually had more bacteria than conventional ones. New regulations say that growers of certified organic produce must carry a certificate that proves their products are pathogen-free.

After the Harvest

Although tainted water and soil splashed onto plants account for a share of contaminated produce, pathogens are often transmitted to produce by people whose hands or tools are dirty with human or animal feces or their own infection. Poor hygiene of food handlers is an important source of contamination for store-bought produce. Some agricultural workers assume that because plants grow in the soil, they don’t need to follow hygienic practices. Moreover, consumers often forget or undervalue the importance of safe handling during food preparation.

Proper postharvest handling is more critical for produce with irregular or wounded surfaces. Any type of injury during any part of production and handling may permit the entry of pathogens such as E. colt O157:H7. Thus, it is critical to discard fruits or vegetables dropped on the floor. Even on unblemished surfaces, microorganisms can attach and form microcolonies, each colony walled behind a tough polysaccharide to form a biofilm. Many types or species of bacteria can occupy a biofilm, which may take hours or days to develop.

Biofilms can form on surfaces such as food-processing equipment and on the food itself. Indeed, most vegetables and some fruits provide ideal conditions for bacterial growth: high moisture content, high nutrient levels and near-neutral pH. Even before you bring them home, common salad vegetables (tomatoes, carrots, lettuce and mushrooms) purchased from grocery stores have been colonized by bacteria; the microcracks and rough surfaces of many types of produce are excellent sites for bacterial attachment and biofilm formation. Bacteria can enter through these cracks and be internalized by the plant tissue, a process that accelerates when warm produce is washed in cool water. Any bacteria in the water can enter the core of the product through the stem scar because of the pressure difference between cold water and warm core. We recommend washing in lukewarm water instead.

Stem scars and other inaccessible places on fruits or vegetables provide surfaces that can protect bacteria or biofilms from washing or sanitizing treatments. Irregular or rough surfaces, such as those found on leafy vegetables and cantaloupes, are ideal places for microbes. There, according to research, bacteria can resist our best efforts to get rid of them. As a result, the most effective strategy is to keep the produce free from harmful pathogens in the first place. If pre- and postharvest practices are stringent enough, we should be able to eat any produce with confidence.

Which Sanitizer?

Although washing doesn’t necessarily remove attached bacteria, growers can get rid of surface pathogens and inhibit decay by using a sanitizing treatment at the time of harvest. The spectrum of treatments includes chemical, physical and nuclear processes, all of which have unique pros and cons.

The most common sanitizers are chlorine based, including chlorine gas (Cl^sub 2^), sodium hypochlorite (NaOCl, also known as household bleach) and calcium hypochlorite (CaClO^sub 2^). The last is cheapest and used most often. Although effective, their antimicrobial activity depends on the amount of free chlorine in solution, which in turn depends on pH, temperature and the amount of organic matter in the water. A fourth form, chlorine dioxide gas (ClO^sub 2^), is relatively unknown, but recent reports suggest that it works particularly well.

As a sanitizing agent, ozone gas (O^sub 3^) can also be very effective, but this depends on concentration, exposure time, relative humidity, temperature, microbial load and the type of fruit or vegetable. Although it is well suited to certain applications, ozone is the most expensive sanitizer approved by regulatory agencies and probably produces more corrosion than any other.

Acetic acid, hydrogen peroxide and peroxyacetic acid are three other disinfectants that show promise for specific uses. Unfortunately, the chemical concentrations needed to lower bacterial counts also make the product look less appealing. Several groups of food scientists are currently working on ways to overcome this drawback.

Calcinated calcium is a new and very promising agent to control pathogenic microorganisms in fresh produce. In one study, this substance (which is made from furnace-blasted bones, whey, shells or coral) was more than 10,000 times as effective as chlorine at reducing the levels of Listeria monocytogenes on tomatoes.

Another recently introduced product is called electrolyzed oxidizing water, which is produced when an electric current passes through dilute saline. This process generates an acidic Hquid that has high oxidation-reduction potential and reactive chlorine compounds. Several studies show it to be effective for eliminating food pathogens in vitro and on kitchen surfaces. Unfortunately, the preparation of electrolyzed oxidizing water requires specialized equipment, and the technique has not gained widespread use.

A good alternative to chemical purification techniques is the use of ultraviolet light at a wavelength of 200-280 nanometers. This so-called ultravioletC (UVC) light offers several advantages over other treatments: It leaves no residue, it doesn’t require a drying step after treatment, and it doesn’t need complex safety equipment. However, UVC treatments do have some disadvantages, including the inability to penetrate tissue and negative effects on quality at high doses.

Among sanitizing treatments, gamma irradiation may be the most effective at eliminating bacteria from intact and fresh-cut produce. However, the dose needed to get rid of pathogens can have an unwelcome effect on pectic substances in the cell walls of the plant, causing the tissue to soften. For this reason, irradiation is not suited for widespread use. Extensive mechanical requirements and public apprehension about the safety of irradiated foods also present obstacles to the application of this technique.

One surprisingly ineffective treatment is plain detergent and water. (Soap, because it contains many trace chemicals, isn’t desirable either.) One study showed no significant differences in the levels of Salmonella and Shigella between produce washed with plain water or with water containing two detergents called Tween 80 and sodium lauryl sulfate. As a result, most consumer groups simply recommend a thorough rinse with lukewarm tapwater.

Putting Safety in Place

Not all sanitizing treatments that succeed in the laboratory will work in a commercial setting. For conventional washing systems, it’s not unusual for a disinfectant to be 100 times less effective at reducing microbial contamination in the field than it was in the laboratory. This failure is often linked to poorly designed equipment that doesn’t do a good enough job of applying the sanitizer to the product.

Indeed, sprays and baths, the most common application methods, are inadequate for some kinds of produce. Better alternatives include vapor-phase treatment and vacuum infiltration, both of which penetrate hard-to-access sites and maximize contact with microorganisms. Some fruits and vegetables can also be surface-pasteurized with steam, hot water or superheated air. Because different strategies target different pathogens, growers in the future may use combinations of disinfectants, such as organic acids with other chemicals, or UV light with a spraying sanitizer.

In the more distant future, pathogens might be controlled by antimicrobial substances produced by other plants or by selected microorganisms. For example, raw carrots and freeze-dried spinach powder both inhibit the growth of Listeria monocytogenes, and some indigenous bacteria can outcompete pathogenic bacteria to prevent its growth. Such “natural” agents may be the next big thing in microbicides and preservatives, although the mechanisms of many of these natural compounds are unclear and require considerable research.

From an industry standpoint, it’s important to emphasize that none of the sanitizing treatments listed above represents a “silver bullet” for ensuring the microbiological safety of fresh produce. Indeed, the best way to get rid of pathogens in produce is to prevent their introduction in the first place. Regardless of the potency of their sanitizing agents, operations that handle fresh produce gently (and hence provide no avenue for pathogen entry) will probably yield safer fruits and vegetables than operations in which nicks and bruises are common.

Tips for Consumers

Preventing the outbreak of foodborne illness is no small task. Fruits and vegetables can become contaminated at any point from the grower’s field to the consumer’s fork. Furthermore, disinfectants alone cannot ensure food safety, and they are particularly ineffective for produce that has punctures or wounds. Additional disinfection technologies are beginning to enter commercial use, but other than irradiation (which has significant disadvantages), no single sanitizing treatment eliminates all pathogens. In the light of such a bleak assessment, what’s a consumer to do?

Fortunately, there are several steps one can take to avoid getting sick from tainted produce. The single best piece of advice is still to wash fruits and vegetables thoroughly before eating them-a practice that can result in a ten-fold reduction in surface contamination. Wash hands with soap before beginning, but just use lukewarm tapwater and a clean cloth or scrub brush on the food. It’s usually best to wash no more than what will be eaten that day to limit microbial growth; however, washing, thoroughly drying (with a cloth or salad spinner) and promptly refrigerating produce is often fine and can sometimes prolong shelf life. Store produce in the refrigerator (except for those products that are not cold tolerant, such as bananas or pineapples). For leafy greens, ready-to-eat salads present no greater risk than lettuce or spinach washed in household kitchens.

Consumers have much more control over their exposure to foodborne pathogens when cooking at home. In preparing fruits or vegetables that will be eaten raw, cut away any damage and the area around the stem scar; these are often sites of microbial colonization. Also, remember that many instances of foodborne illness caused by fresh produce actually begin with cross-contamination from raw meat. Foodborne pathogens are much more likely to survive and thrive in uncooked meat than in fruits or vegetables, which explains why it is much safer to eat raw produce than to eat raw meat. Hands, surfaces and kitchen tools should be washed thoroughly with soap before and after preparing food, and it is prudent to wash hands frequently while cooking-most especially after handling meats or using the toilet.

Overall, it’s important to put the risk of eating produce in a larger context. Fresh fruits and vegetables are no riskier than other fresh foods as sources of foodborne pathogens, and eating a salad is certainly safer than driving to work. Furthermore, many forms of produce confer remarkable health benefits on people who eat them. Given these benefits, avoiding fresh fruits and vegetables is probably riskier than enjoying them-even if you still eat unwashed fruit with grubby fingers.