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	The number of reported foodborne outbreaks attributable to fruits and vegetables has been rising in recent years, both in the United States and abroad.
	It's difficult to determine the reason for the rise in outbreaks because virtually every aspect of the produce industry has changed during the past 20 years.
	In the United States, domestic produce is contaminated mainly by animals, leading to E. coli and Salmonella infections; imported foods are also associated with human pathogens—e.g., Shigella, Norovirus, and Hepatitis A.
	New infections are emerging in other countries, such as foodborne Chagas disease.
	Produce can become contaminated by infected food workers; in the farm environment; through irrigation waters; during processing and packaging, particularly of ready-to-eat items.
	Food safety efforts are ongoing, but much remains to be done; ideally, scientists need to find ways to prevent contamination before it occurs.

Photo: Color-enhanced scanning electron micrograph showing Salmonella typhimurium (red) invading human cells. By permission, Rocky Mountain Laboratories, NIAID, NIH.

It seems that hardly a month goes by without a report of some kind of food-related illness outbreak. On April 11, 2008, following detection and investigation by state health departments and the Centers for Disease Control and Prevention (CDC), the U.S. Food and Drug Administration announced that 21 people in 13 states were diagnosed with a Salmonella infection caused by the same strain of the organism found in a recently recalled batch of dried cereal. On March 22, following a similar investigation, the FDA warned that cantaloupes from a Honduran company were contaminated with Salmonella; 50 illnesses in 16 states and nine illnesses in Canada were linked to the consumption of contaminated melons. On February 7, the FDA issued an expanded recall of canned vegetables that may have been contaminated with Clostridium botulinum.

Michael Doyle explains the threat of pathogens carried by fresh produce. video

Outbreaks attributable to fruits and vegetables, in particular, have been rising steadily in recent years, according to the prominent scientists who met at the Academy on April 21, 2008, to discuss foodborne illness. Today, produce and plant-associated products are "leading vehicles" of foodborne illnesses in the United States—responsible for more than half of illnesses associated with foodborne outbreaks between 1998 to 2004, according to Michael Doyle a food microbiologist and director of the University of Georgia Center for Food Safety.

To put the rise in contamination in perspective:

• From 1973–1997, 190 foodborne outbreaks were linked to fresh produce, causing 16,058 illnesses, 598 hospitalizations, and eight deaths.
• From 1998–2004, 384 outbreaks (28 multi-state) were linked to produce items, causing 15,856 illnesses, 716 hospitalizations, and 15 deaths.

This represents "a clear trend of outbreaks getting bigger and more common," observed Robert Tauxe of the CDC.

Moreover, the upswing in produce-related outbreaks is a global phenomenon. And although in the United States, consumers are especially aware that some imported food products are produced under unsanitary conditions, the fact is, contamination is also occurring domestically, the speakers emphasized.

Why the increase? It's almost impossible to tell because "virtually nothing is the same about the produce industry between today and what it was 20 years ago," said the FDA's Robert Buchanan.

Different types of infections seem to be associated with domestic (U.S.) versus imported foods, though that may be changing as pathogens introduced from abroad establish themselves in the United States. Right now, said Buchanan, domestic produce is contaminated mainly by animals (zoonotic diseases), leading to infection by E. coli and Salmonella. Imported foods are also associated with human pathogens—for example, Shigella, Norovirus, and Hepatitis A.

Several outbreaks associated with raspberries imported from Guatemala were linked to Cyclospora, a disease of developing countries spread by ingestion of food or water contaminated by an infected stool.

"It seems you're getting not just fresh-pressed jungleberry juice, but also fresh-pressed T. cruzi."

Globally, new food-related infections are emerging, added Tauxe. For example, in Brazil, foodborne Chagas disease is becoming more common. Chagas disease is a potentially life-threatening infection caused by the blood-sucking parasite, Trypanosoma cruzi. In 2007, eighteen outbreaks were traced back to fresh-pressed acaí (jungleberry) juice, which is increasingly consumed as an energy drink. "It seems you're getting not just fresh-pressed jungleberry juice, but also fresh-pressed T. cruzi—'bug juice,' literally," said Buchanan. T. cruzi also survives in fresh sugarcane juice, where it was responsible for a 1968 outbreak.

Scientists are also discovering "cross-over pathogens" that infect both plants and humans, Tauxe commented. For example, a pathogen that infects young onions also causes severe chronic infections in patients with cystic fibrosis, making it "a pediatric opportunistic infection of both onions and people."

And studies of human clinical isolates of Pseudomonas aeruginosa, a bacterium responsible for hospital-acquired pneumonia, showed that the bug contains virulence genes for both human and plant hosts. "This suggests that we have more in common with onions and other plants than we might think," said Tauxe.

Food can become contaminated in myriad ways throughout the production, packaging, and distribution processes.

Infected workers

Sanitation practices differ throughout the world, and there are no universal standards among food workers, Doyle observed. For example, an outbreak of Hepatitis A associated with onions was traced back to farms in Mexico where children accompany their parents into the fields during harvesting; the children play in—and defecate on—the onions over the course of the day.

There are also plenty of problems on the domestic front. A recent U.S. survey revealed that although food workers knew the appropriate steps to take to help prevent contamination, 23% (4.4 million) did not wash their hands; 33% (6.3 million) did not always change gloves between touching raw meats and ready-to-eat foods; 60% (11.4 million) did not wear gloves when touching ready-to-eat food; 53% (10.1 million) did not consistently use a thermometer; 4.7% (900,000 nationally) worked while ill with vomiting or diarrhea. Reasons for not complying included lack of time, lack of staff, or thinking their work was at low risk for causing illness.

Farm environment

Buchanan noted that the farm environment is replete with animals that are reservoirs for foodborne pathogens. Salmonella is common in fruit flies and E. coli is found in pigs and deer. Investigations of a recent outbreak of tomato-associated illness on the east coast of the United States revealed that regions that are part of the flyway for migrating birds were among those hardest hit by Salmonella infection. Moreover, toads in Florida were suspected of carrying Salmonella in that outbreak. Deer were identified as the likely source of contamination in an apple cider outbreak, and pigs were implicated in a major spinach outbreak.

Rural environment/economies of scale

The advent of huge farms in the United States and elsewhere also contributes to outbreaks, according to Buchanan. A typical field in California's Salinas Valley yields about a quarter of a million heads of lettuce that will be picked all at one time. "The scale is enormous, which is great for economics, but if you make a mistake in terms of food safety, that's a lot of lettuce to deal with," he commented.

The likelihood of that happening is influenced by multiple factors. For one thing towns, cities, suburbs, and farms with cattle are all intermingled among the lettuce fields. "You can walk across the street from a store or home right into a lettuce field and vice versa," Buchanan explained. Every available piece of land is used for some sort of food-related activity. So land in a hilly area that is not suitable for produce cultivation is used for cattle production. The cattle are right above the fields, and it's easy to imagine how gravity works to send E. coli down the hill.

Irrigation

This irrigation canal, which consistently contained E. coli when tested, is located approximately 100 yards from a cattle dairy. Click to enlarge.

Contamination also spreads from farm to farm via irrigation waters. Most of the fruits and vegetables produced in the Western United States and Mexico are irrigated because there's not enough rainfall to support crop growth—and there are no standards for irrigation waters, explained Charles Gerba of the University of Arizona.

Irrigation canals are complex, man-made systems through which water may travel hundreds of miles. Fifty years ago, when many of the systems were built, the water flowed mainly through croplands. But now, the water has to be moved through major cities that didn't exist when the irrigation canals were originally constructed. The "urban-rural" interactions that take place are having an effect on the waters, Gerba warned.

A study by Gerba's group of water in the irrigation canals in Yuma, Arizona, yielded the following: about 21% of samples had Salmonella; 55% had Campylobacter, probably from migrating birds; 20% had Cryptosporidium, presumably from cattle; 20% had Norovirus, probably from the water originating in recreational areas; and 5% had Giardia, probably from humans. And when it comes to irrigation waters in developing countries, "you can find just about anything," Gerba said.

Organic farms are not exempt from contamination either, Gerba stated. In the Yuma area, both organic and non-organic farms get their water from the same sources. Even when organic farmers use a groundwater source, the water passes through an irrigation canal for a half mile or so before it gets to the farm, he said.

Infiltration/internalization

Although people commonly think pathogens are present only on the surface of produce, in fact, in many cases, they are taken up and absorbed right into the plant. "It's important to look at a product as a pathogen sees it, not as a human," Buchanan explained. For example, people often worry about contamination of non-acidic foods such as cantaloupes, not acidic foods such as tomatoes, apples, and oranges. Yet, a pathogen looking at an orange may see not only the acidic juice sac, but also the nearby integra, which is neutral in pH. And the pathogen can grow quite well in the integra.

Dye studies show that the stem scar is a portal of entry into mangos, grapefruits, and oranges. Click to enlarge.

There are a number of potential portals of entry by which pathogens can get inside plants (infiltration), and persist (internalization), resulting in contaminated food products that can't be decontaminated by current methods. In an apple, pathogens can enter in the calyx, where the flower was, and wend their way up into the core. Experiments in sprouts have shown that if Salmonella or E. coli are placed on the seed coat, once sprouts appear, the pathogens will be picked up by root hairs, and go on to invade the young plant and colonize all its tissues (the plant remains unharmed).

In other work, researchers painted Salmonella onto the flowers of tomato plants purchased at a nursery; certain strains were found inside the tomatoes a month later. "This suggests that Salmonella can go in with the pollen tube, ride that down to the ovial at the time of fertilization, and then persist and appear in the new fruit. That's really pretty clever behavior," Buchanan said.

Infiltration also occurs during processing and packaging. Tomatoes and other fruits move through cold water transport systems to reduce bruising and maintain quality. Although the water contains chlorine, there's not enough to kill all the pathogens (using more chlorine would mean adding unacceptable levels of the disinfectant). And so micro-organisms spread through the water from one piece of fruit to another. In addition, there's a "suction effect" when fruit goes from ambient temperature into a cold environment; the fruit contracts, creating a pressure differential with the surrounding water; to balance that pressure, it sucks in water—and if the water contains bacteria, they're sucked up into the fruit, as well.

"There are many other ways for pathogens to get into the intact fruit or inside leafy greens ... so these are not sterile products," Buchanan stressed.

Wounded produce

Whenever produce is peeled, cut, diced, or otherwise processed to make it convenient and ready-to-eat, the produce is effectively wounded, explained Doyle. The plant tissue breaks down, making it easier for bacteria to attach to the open surfaces. At the same time, a tremendous amount of liquid is released, which serves as a nutrient source for the attached bacteria. And that same liquid can neutralize chlorine or other disinfectants used to treat the produce, rendering them ineffective.

Finally, at the grocery store, bagged fresh produce may sit out in the aisle unrefrigerated, especially if the store is trying to sell it the same day. This "temperature abuse" increases the growth of pathogens, said Doyle. Because the bagged produce is ready-to-eat, consumers are exposed directly to any pathogens it may contain.

What are governments doing to stem outbreaks and enhance food safety? With respect to imported food, inspectors can look at the production and processing systems of the country of origin, an approach that the European Union is taking. Imported products can also be screened at the point of entry, which the United States is attempting to do, or a country can use some combination of the two strategies, explained Ewen Todd of Michigan State University. In addition, he pointed out that the companies that are importing the foods should also be going to the countries of origin and "making sure that they understand what's going into their products," he stressed.

Myriad other issues need to be addressed when trying to establish good agricultural practices, said Todd, touching on many of the areas of concern raised in the previous talks. These include crop production water, manure, animal fecal contamination, worker health and hygiene, field and harvest sanitation, packing facilities, post-harvest water during packing, storage and distribution, and fresh-cut processing.

Trying to ensure safety in even one of these areas is not straightforward. An example is microbial testing. It would seem logical to prevent outbreaks by testing produce before it goes to market. But, as Buchanan pointed out, testing a fruit or vegetable effectively destroys it, so if you tested all the food, you'd have none left. Yet, testing one piece here or there doesn't work either. In any given bin of produce, one piece may be free of contamination while the piece right next to it harbors a pathogen. One way to get around the problem is to take "smarter samples," he said. That might mean taking larger samples—for example, sampling an entire bin by washing all the products in it and looking at the resulting water sample.

If 5% of a group of 40 units are contaminated and 5 samples are tested, there is a 77% chance that the contamination will go undetected. Click to enlarge.

Other strategies are in the works. Various international entities such as the Codex Alimentarius Commission of the Food and Agriculture Organization of the United Nations and the World Health Organization, and the World Organization for Animal Health are generating traceability principles and standards; bar codes, RFID (radiofrequency identification), and other technologies are being developed to facilitate rapid traceback and recalls. The ultimate goal would be to have a universal system that allows rapid, accurate traceback anywhere in the world.

But plenty remains to be done, especially in the area of prevention, CDC's Tauxe pointed out. Produce is often eaten uncooked; unlike meat, you don't put lettuce in the oven until it's 160°F and let the juices run clear. "Washing might be logical, but it turns out that it removes very few pathogens," he said. Tauxe went on, "Right now prevention measures are based more on common sense than on the limited science that's available. My question is, do we know enough to prevent contamination from occurring in the first place, because that's clearly what we need to do."

With that sobering thought in mind, event co-organizer Barry Kreiswirth of the Public Health Research Institute undoubtedly voiced what many conference attendees were thinking at the end of the sessions. "I'm amazed, given the amount of food we make and distribute, that we're all not sick every day."

Use the search utility within individual slideshows with audio to find additional details on each presentation. (The Search function to the left does not search the text of the slides themselves.)

Presentations

		From Wild Pigs and Spinach to Tilapia and Asia: Current Microbiological Food Safety Concerns Michael Doyle slides w/ audio				Emerging Foodborne Infections: The Plant Story Robert Tauxe slides w/ audio
		Emergence of Produce as a Vehicle for Foodborne Disease Robert Buchanan slides w/ audio				The Ecology of Pathogens Associated with Domestic and Imported Produce Charles Gerba slides w/ audio
		Improving the Safety of Imported Food Ewen Todd slides w/ audio

Web Sites

Centers for Disease Control and Prevention: Food Safety Office
The Web site of the U.S. CDC's food safety office has information on diseases/pathogens, environmental hazards, outbreak investigations, and more.

U.S. Department of Agriculture: Food Safety Information Center
The U.S. Department of Agriculture has a National Agriculture Library that provides food safety information to educators, industry, researchers, and the general public.

U.S. Food and Drug Administration: Center for Food Safety & Applied Nutrition
The Center for Food Safety and Applied Nutrition has a wealth of information on its Web site detailing program areas such as pesticides and chemical contaminants, produce safety, and imports.

Foodsafety.gov
This Web site serves as the gateway to government food safety information.

Articles

Global increase in infected food

Batz MB, Doyle MP, Morris G Jr, et al; Food Attribution Working Group. 2005. Attributing illness to food. Emerg. Infect. Dis. 11: 993-999.

Buchanan RL. 2004. 1st International Conference on Microbiological Risk Assessment: foodborne hazards—what we heard. J. Food Prot. 67: 2072-2074.

CDC. 2008. Multistate outbreak of human Salmonella infections by contaminated dry dog food—United States, 2006-2007. MMWR 57: 521-524.

Chittick P, Sulka A, Tauxe RV, Fry AM. 2006. A summary of national reports of foodborne outbreaks of Salmonella Heidelberg infections in the United States: clues for disease prevention. J. Food Prot. 69: 1150-1153.

Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV. 2004. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J. Food Prot. 67: 2342-2353.

Vojdani JD, Beuchat LR, Tauxe RV. 2008. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J. Food Prot. 71: 356-364.

Types of infections

Erickson MC, Doyle MP. 2007. Food as a vehicle for transmission of Shiga toxin-producing Escherichia coli. J. Food Prot. 70: 2426-2449.

Zhang G, Ma L, Patel N, Swaminathan B, et al. 2007. Isolation of Salmonella typhimurium from outbreak-associated cake mix. J. Food Prot. 70: 997-1001.

Modes of infection

Eblen BS, Walderhaug MO, Edelson-Mammel S, et al. 2004. Potential for internalization, growth, and survival of Salmonella and Escherichia coli O157:H7 in oranges. J. Food Prot. 67: 1578-1584.

Islam M, Morgan J, Doyle MP, et al. 2004. Persistence of Salmonella enterica serovar typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathog. Dis. 1: 27-35.

Greig JD, Todd EC, Bartleson CA, Michaels BS. 2007. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved. J. Food Prot. 70: 1752-1761.

Todd EC, Greig JD, Bartleson CA, Michaels BS. 2007. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 2. Description of outbreaks by size, severity, and settings. J. Food Prot. 70: 1975-1993.

Todd EC, Greig JD, Bartleson CA, Michaels BS. 2007. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories. J. Food Prot. 70: 2199-2217.

Food-safety efforts

Stine SW, Song I, Choi CY, Gerba CP. 2005. Application of microbial risk assessment to the development of standards for enteric pathogens in water used to irrigate fresh produce. J. Food Prot. 68: 913-918.

Edelson-Mammel SG, Whiting RC, Joseph SW, Buchanan RL. 2005. Effect of prior growth conditions on the thermal inactivation of 13 strains of Listeria monocytogenes in two heating menstrua. J. Food Prot. 68: 168-172.

Stine SW, Song I, Choi CY, Gerba CP. 2005. Effect of relative humidity on preharvest survival of bacterial and viral pathogens on the surface of cantaloupe, lettuce, and bell peppers. J. Food Prot. 68: 1352-1358.

From the Academy

eBriefings

Antipoverty vaccines: strategies against neglected tropical diseases, featuring Peter Hotez et al. 2008. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group.

Risks and realities: community-acquired diseases in New York and New Jersey, featuring Alan Neaigus et al. 2007. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group.

Invasive Aspergillosis: new approaches against a dangerous fungal infection, featuring David Denning et al. 2006. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group.

Flu preparedness: lessons learned, action plans, and new directions, featuring Peter Palese et al. 2006. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group.

Annals Volumes

Frazier TW, Richardson DC, eds. 1999. Food and Agricultural Security: Guarding against Natural Threats and Terrorist Attacks affecting Health, National Food Supplies, and Agricultural Economics. Annals of the New York Academy of Sciences, Vol. 894.

Gibbs EPJ, Bokma BH, eds. 2002. The Domestic Animal/Wildlife Interface: Issues for Disease Control, Conservation, Sustainable Food Production, and Emerging Diseases. Annals of the New York Academy of Sciences, Vol. 969.

Tucker WT, Ferson S, Finkel AM, Slavin D, eds. 2008. Strategies for Risk Communication: Evolution, Evidence, Experience. Annals of the New York Academy of Sciences, Vol. 1128.

Michael Doyle, PhD
University of Georgia
e-mail | web site | publications

Michael Doyle is Regents Professor of Food Microbiology and director of the Center for Food Safety. His research focuses on bacterial foodborne pathogens, including E. coli O157:H7 and other serotypes of enterohemorrhagic E. coli, Salmonella spp., Campylobacter jejuni, Listeria monocytogenes, Staphylococcus aureus, and Clostridium botulinum.

Robert V. Tauxe, MD, MPH
U.S. Centers for Disease Control and Prevention
e-mail | web site | publications

Robert Tauxe is deputy director of the CDC Division of Foodborne, Bacterial, and Mycotic Diseases. He holds an MD from Vanderbilt Medical School and a Masters in Public Health from Yale University. Following a residency in internal medicine at the University of Washington, he joined the CDC staff in 1985. His work has focused on bacterial enteric diseases, epidemiology and pathogenesis of infectious diseases, epidemiologic and clinical consequences of bacterial genetic exchange, antimicrobial use and resistance to antimicrobial agents, and the teaching of epidemiologic methods. He has worked in Belgium, Mali, Rwanda, Peru, and Guatemala, and has supervised numerous overseas epidemiologic investigations.

Robert Buchanan, PhD
Center for Food Safety and Applied Nutrition, FDA
e-mail | web site | publications

Robert Buchanan is senior science advisor and director of the Office of Science at the Center for Food Safety and Applied Nutrition. Before moving to the FDA, Buchanan was a senior investigator with the U.S. Department of Agriculture's Agricultural Research Service (ARS), stationed at the ARS Eastern Regional Research Center in Philadelphia. He served in various orther positions in USDA including deputy administrator for science and technology for the Food Safety and Inspection Service.

Prior to his USDA career, Buchanan served as an associate professor at Drexel University. He is the recipient of numerous professional awards including the University of Wisconsin Fraiser Award, the Institute of Food Technologist's Bauermann Award, and the ARS Outstanding Scientist of the Year Award. He is a fellow of the American Academy of Microbiology and a member of both the National Advisory Committee on Microbiological Criteria for Foods and the International Commission for Microbiological Specifications for Foods. He is also a member of numerous professional organizations and serves as a contributing editor for Food Microbiology and a member of the board of editors for the Journal of Food Safety and the Journal of Food Protection.

Buchanan received his PhD in microbiology from Rutgers University, and post-doctoral training at the University of Georgia.

Charles Gerba, PhD
University of Arizona
e-mail | web site

Charles Gerba is a professor of environmental microbiology in the Departments of Microbiology and Immunology, Epidemiology and Biostatistics, and Soil, Water and Environmental Science at the University of Arizona. He has been involved in studying the environmental transmission of disease-causing microorganisms for more than 30 years and has published more than 500 scien tific articles in this area.

Gerba has served on the Pima County (Ariz.) Board of Health and as a consultant to the World Health Organization, the United States Environmental Protection Agency, and the Centers for Disease Control and Prevention. He is a member of the American Academy of Microbiology. Gerba earned his PhD from the University of Miami, Coral Gables, Fla.

Ewen Todd, PhD
Michigan State University
e-mail | web site

Ewen Todd is director of Michigan State University's National Food Safety and Toxicology Center. Through his work as a research scientist, he has been involved with the reporting and surveillance of foodborne disease, developed methods to detect E. coli 0157:H7, shiga toxin-producing E. coli and Salmonella in food, estimated the number and cost of cases of foodborne disease in Canada and the United States, determined the impact of seafood toxins, and developed quantitative risk assessments for pathogens in foods.

Todd received his PhD in bacteriology from the University of Glasgow, where he was an assistant lecturer. He served as chairman of the Foodborne Disease Reporting Centre and co-chairman of the Botulism Reference Centre, both within the Health Products and Food Branch in Ottawa.

Todd has encouraged foodborne disease prevention and control strategies by promoting the Hazard Analysis Critical Control Points (HACCP) system and worked with Agri-Food Canada to develop model HACCP plans for 30 products. He has also participated in WHO and FAO working groups and consultations in Geneva, Rome, Cambodia, and China.

Marilynn Larkin is a medical editor, journalist, and videographer based in New York City. Her work has frequently appeared in, among others, The Lancet, The Lancet Infectious Diseases, and Reuters Health's professional newswire. She has served as editor of many clinical publications and is author of five medical books for general readers as well as Reporting on Health Risk, a handbook for journalists. She is currently head of publications for The Society for Biomolecular Sciences.

In 2004, Ms. Larkin started her own fitness consulting company (www.mlarkinfitness.com), and developed a class, Posture-cize, that helps people improve their posture, increase productivity, and reduce injury.