University of Florida

Salmonella & Tomatoes: Q&A for Consumers

Teplitski, M.,1 Schneider, K.,2 and Danyluk, M.D.3

The recent outbreak of salmonellosis linked to the consumption of tomatoes--as well as previous outbreaks of gastrointestinal illnesses caused by E. coli O157:H7 linked to leafy greens--raises questions about microbiological safety of fresh fruit and vegetables. In this document, we attempt to synthesize recent research to address some of the more common questions.

Q. Is eating fresh produce risky?

Each one of us comes in contact with various pathogens throughout the day. The most recent outbreak of produce-associated salmonellosis so far has been linked to over 220 cases in 23 states. Approximately 30 percent of people in these states report consuming fresh tomatoes on a daily basis. Therefore, one out of 3.7 million people who consume tomatoes daily in these states have developed salmonellosis-like signs.

These calculations show that most of us ingest or inhale hundreds of pathogens daily without ever becoming sick. Typically, at least several thousand cells of Salmonella are required to cause salmonellosis in healthy adults, although one outbreak of salmonellosis resulted from consuming as few as four Salmonella cells per serving of ice cream (6).

Q. I had diarrhea this morning. Is that salmonellosis?

Only your doctor can diagnose salmonellosis. Diarrhea symptoms associated with salmonellosis are much more severe than those of an upset stomach. Other symptoms of salmonellosis include headaches, abdominal pain, nausea and fever. Gastroenteritis usually resolves itself within a few days without antibiotic treatment in otherwise healthy adults. Those who are at higher risk--pregnant women, children, elderly, people who have undergone recent antibiotic therapy or immunosuppression treatment--should consult their physicians at the first signs of the disease.

Q. How do Salmonella, E. coli O157:H7, and other human pathogens contaminate tomatoes and other fruits and vegetables?

There is no quick answer to this question. There is an ongoing scientific discussion regarding the most likely routes of produce contamination. Conceivably, produce could be contaminated during cultivation, harvest, cleaning, washing and distribution. In the field, fruits and vegetables can be contaminated by coming in contact with animal manure or poultry litter that was improperly composted. Bird, animal, and insect droppings can occasionally land on produce in the field and deposit pathogens on surfaces. Improper hygiene during handling of fruits and vegetables can also be an important factor in breaching the microbiological safety of produce. Cross-contamination in retail and during food preparation at home and in restaurants has also been documented (3).

To date, there is no consensus on whether Salmonellaand E. coli O157:H7 only contaminate surfaces of fruits and vegetables, or whether these bacteria are able to efficiently colonize internal parts of the plant. Controlled studies using high doses of bacteria suggest that Salmonella and E. coli O157:H7 are able to contaminate produce in the field by colonizing plant root surfaces from infested soil or seeds, and bacteria then spread to all parts of the plant (9). In controlled field studies when E. coli and Salmonella were artificially mixed with the animal manure, bacteria were able contaminate all parts of the plants (1, 7, 8, 10).

It is also possible that Salmonella and E. coli O157:H7 can directly colonize leaves and stems by entering through wounds or stomata (openings on leaves through which plants "breathe"). While these studies provide hints about potential routes of infection, there is still no clear indication which, if any, of these contamination routes have led to an outbreak (reviewed in reference 4).

Q. Can consumers visually inspect produce to identify fruits and vegetables that are contaminated with Salmonella or E. coli O157:H7?

No. Even in studies in which fruits and vegetables were artificially contaminated with high doses of Salmonella or E. coli O157:H7, the produce did not show signs of spoilage, did not have an unpleasant odor, and did not differ in appearance from uncontaminated fruit and vegetables. This may be due to the fact that neither Salmonella nor E. coli O157:H7 have evolved as plant pathogens and cannot efficiently degrade plant tissues or cause visible spoilage of produce.

While Salmonella and E. coli O157:H7 cannot cause produce decay, one study has demonstrated that fresh or cut fruits and vegetables sampled from various supermarkets are twice more likely to harbor Salmonella if they are already affected by "bacterial soft rot" (14). Soft rot is a produce decay caused by plant pathogenic bacteria. The best advice, therefore, is to purchase intact, uninjured fruit and vegetables.

FDA also maintains an updated Web site with the most recent information on the types of tomatoes that are being recalled: Salmonellosis Outbreak in Certain Types of Tomatoes.

Q. Is there anything consumers can do at home to reduce the risk of infection?
  1. When selecting fruits and vegetables at the market, do not pick damaged produce, and avoid selecting those that are too soft or have translucent skin. Even though Salmonella and E. coli O157:H7 do not cause produce decay, damaged vegetable are more likely to also contain these human pathogens. Avoid picking fruits and greens that are soiled.
  2. Store your produce dry in a cool place. Although storing at cooler temperatures does not consistently reduce any potential contamination, it helps to prevent pathogens from multiplying (15).
  3. Never soak your vegetables in water. This may increase the chance that any bacteria present on the surface may infiltrate into the inner tissues.
  4. Fruits and vegetables that have been minimally processed--i.e., thoroughly washed and brushed, cut, sliced, peeled, lightly cooked, etc.--should be refrigerated and only for a limited time.
  5. Clean your refrigerator. Regularly wipe refrigerator shelves and crispers with a household cleaner.
  6. Washing produce is an important way to remove some contamination on the surface of fruits and vegetables. Thoroughly washing produce in warm water with common detergents reduces--but does completely eliminate--bacteria on surfaces of tomatoes (12). When washing fruits and vegetables at home, consumers should make sure that detergents are food-grade, are approved by FDA for this purpose, and do not contain any harmful chemicals. Fruits and vegetables should be washed under clean running warm water. Do not wash your vegetables or fruits in bleach solutions; they are not considered safe for consumption.

    Wash fruits and vegetables immediately prior to eating them. Washing removes fruits’ natural protective wax coating, and brushing abrades the skin, reducing the shelf life of produce and creating potential routes for contamination. Be aware that washing is not likely to remove Salmonella or other human bacterial pathogens that may have gotten inside. Washing is only modestly effective in removing pathogens from vegetables with rough surfaces (cantaloupes, strawberries, broccoli, cauliflower, etc.).
  7. When slicing tomatoes, cut out the stem scar (the corky area on top of a tomato fruit that was attached to the stem). Studies using artificial contamination show that after tomatoes are picked and soaked in a suspension containing Salmonella, the stem scar appears to contain higher numbers of bacteria (15).
  8. When preparing fruits and vegetables at home, avoid cross-contamination by separating fruits and vegetables from meats, poultry, seafood, and those vegetables (potatoes, leeks, etc.) and cucurbits (melons, squash) that are normally soiled.
Q. I only buy organic produce.  This pretty much means that it is safe, right?

Not necessarily. While organic produce may not have pesticide residues, it does not mean that it is free of Salmonella or other microbial contaminants. Because organic market is still quite limited, it is difficult to directly compare microbiological safety of organic and conventional produce. One could suspect, however, that because organic farmers rely on manure and poultry litter to fertilize their fields, there is a chance of inadvertently contaminating vegetables in cases when manure and poultry litter are not properly composted. A small-scale survey of organic and conventionally produced vegetables in Minnesota supported this hypothesis (11).  

We note, however, that organic market is very limited at this point, and there is an on-going scientific debate about the safety of organic produce. This debate is exemplified by an on-going exchange in Nature, one of the flagship scientific publications: Response to "Blame factory farming, not organic food".

Q. I always have a drink of alcohol with my food. This keeps me safe from bacteria, right?

There is no direct answer to this question. Generally, consumption of alcohol is considered to suppress the immune system. The immune systems of "sober" mice and those that were fed ethanol responded differently when they were exposed to Salmonella (12). It should be noted that unlike humans and other primates, mice respond differently to a Salmonella infection and develop typhoid fever-like symptoms when exposed by non-typhoidal Salmonella (13).  

A very limited survey of 51 persons who were exposed to tomatoes contaminated with a Salmonella during an outbreak in Spain suggests that having a drink may have modestly reduced the risk of getting infected (2).

Q. What are scientists doing to ensure safety of produce?

Scientists around the world and here at the University of Florida/IFAS are working to improve safety of fresh fruits and vegetables. These include: 1) studies on removing reservoirs of pathogens in the field, greenhouses, washing and packing facilities; 2) the fate of Salmonella and E. coli O157:H7 on or in fresh fruits and vegetables following harvest; 3) investigations into mechanisms by which Salmonella and E. coli O157:H7 infect and attach to fruits and vegetables in order to then disrupt these behaviors with new formulations of washes or sprays; 4) efforts to improve conditions and hygiene of workers involved in growing, harvesting and processing of fruits and vegetables; 5) DNA-fingerprinting techniques to quickly identify a pathogen and link it to a potential source of infection.

There are new formulations of vegetable washes that are being developed. For example, Harris and colleagues developed a prototype wash solution for tomatoes that contains water, oleic acid, glycerol, ethanol, potassium hydroxide, sodium bicarbonate, citric acid, and distilled grapefruit oil. This wash reduced surface contamination of tomatoes with Salmonella by 100-10,000 fold (4). A formulation for an edible film that contains glycerin, soy protein, and malic acid with the potential to prevent growth of Salmonella and other pathogens was registered with the U.S. Office of Patents and Trademarks (6). Consumers should be warned, however, not to attempt to concoct similar formulations at home; before washes or edible films are approved by FDA, they undergo rigorous testing to ensure that each component of the wash is safe. 

The Florida tomato industry has recently instituted the Tomato Good Agricultural Practices (T-GAPs) program. As a part of the program, educators at the University of Florida are providing food safety training to all Florida growers and processors. Strict adherence to GAP principles also ensures the safest product possible. The Florida Department of Agriculture and Consumer Services is enforcing a new rule that requires all tomatoes produced in Florida have to be treated with a sanitizer before they can be marketed.

Therefore, unsurprisingly, FDA scientists certified tomatoes produced in Florida as "safe-to-eat": Bronson Announces Florida Tomatoes Deemed Safe By FDA--FDACS.

Q. Why is it taking so long to identify where contaminated tomatoes come from? How do scientists track the source of pathogens, anyway?

Linking an outbreak to a specific source will require some time. First, epidemiologists need to identify what patients have in common (i.e., Did they eat the same type of food? Did they go to the same restaurant?, etc). Once the source of "pathogen X" is narrowed down (i.e., "food A" or "restaurant chain Y"), scientists will attempt to identify whether a specific batch of the product was contaminated. 

Fresh produce--such as tomatoes--often travel long distances before being sold or consumed. Tomatoes are not individually labeled when being shipped, and they are often mixed with other tomatoes of similar variety and ripeness--but from other growing regions--before being sold. This mixing process makes it very difficult for epidemiologists to pinpoint the source or a farm that produced the tomatoes that were contaminated.   

Once the "pathogen X" is identified in a sample of "food A", geneticists will use specific DNA fingerprints of the pathogen to compare it to the known DNA fingerprints of other isolates of the same pathogen to see whether there is a close match. Once these genetic fingerprints of different isolates of the pathogen are matched, they could be used as one piece of evidence linking an outbreak to a specific field or a packing facility.

Additional information about tomato safety can be found at the following Web pages:

Several EDIS publications detail steps that each consumer can take at home to reduce the risk of various gastrointestinal illnesses:

References
  1. Barak, J. D., and A. S. Liang. 2008. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS ONE 3:e1657.
  2. Bellido-Blasco, J. B., A. Arnedo-Pena, E. Cordero-Cutillas, M. Canos-Cabedo, C. Herrero-Carot, and L. Safont-Adsuara. 2002. The protective effect of alcoholic beverages on the occurrence of a Salmonella food-borne outbreak. Epidemiology 13:228-30.
  3. Bidol, S. A., E. R. Daly, R. E. Ricker, T. A. Hill, T. H. Taylor, M. F. Lynch, J. A. Painter, C. R. Braden, P. A. Yu, L. Demma, C. Barton Behravesh, C. K. Olson, S. K. Green, A. M. Schmitz, D. D. Blaney, and M. D. Gershman. 2007. Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in restaurants --- United States, 2005--2006. CDC Morbidity and Mortality Weekly Report 56:909-911.
  4. Heaton, J. C., and K. Jones. 2007. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J Appl Microbiol.
  5. Hennessy, T. W., C. W. Hedberg, L. Slutsker, K. E. White, J. M. Besser-Wiek, M. E. Moen, J. Feldman, W. W. Coleman, L. M. Edmonson, K. L. MacDonald, M. T. Osterholm, and T. I. Team. 1996. A national outbreak of Salmonella enteritidis infections from ice cream. N Engl J Med 334:1281-6.
  6. Hettiarachchy, N. S., and E. Satchithanandam. 2003. Organic acids incorporated edible antimicrobial films. US Patent 10/657,692
  7. Islam, M., J. Morgan, M. P. Doyle, S. C. Phatak, P. Millner, and X. Jiang. 2004. Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl Environ Microbiol 70:2497-502.
  8. Islam, M., J. Morgan, M. P. Doyle, S. C. Phatak, P. Millner, and X. Jiang. 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.
  9. Klerks, M. M., M. van Gent-Pelzer, E. Franz, C. Zijlstra, and A. H. van Bruggen. 2007. Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enterica serovar Dublin. Appl Environ Microbiol 73:4905-14.
  10. Mukherjee, A., D. Speh, and F. Diez-Gonzalez. 2007. Association of farm management practices with risk of Escherichia coli contamination in pre-harvest produce grown in Minnesota and Wisconsin. Int J Food Microbiol.
  11. Mukherjee, A., D. Speh, E. Dyck, and F. Diez-Gonzalez. 2004. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot 67:894-900.
  12. Sibley, D. A., N. Osna, C. Kusynski, L. Wilkie, and T. R. Jerrells. 2001. Alcohol consumption is associated with alterations in macrophage responses to interferon-gamma and infection by Salmonella typhimurium. FEMS Immunol Med Microbiol 32:73-83.
  13. Tsolis, R. M., R. A. Kingsley, S. M. Townsend, T. A. Ficht, L. G. Adams, and A. J. Baumler. 1999. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections. Adv Exp Med Biol 473:261-74.
  14. Wells, J. M., and J. E. Butterfield. 1997. Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Disease 81:867-872.
  15. Zhuang, R. Y., L. R. Beuchat, and F. J. Angulo. 1995. Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Appl Environ Microbiol 61:2127-31.
Footnotes
  1. Max Teplitski, assistant professor, Soil and Water Science Department, Florida Cooperative Extension Service, Emerging Pathogens Institute, Institute of Food and Agricultural Sicences (IFAS), University of Florida, Gainesville, FL 32611-0290
  2. Keith R. Schneider, associate professor, Department of Food Science and Human Nutrition, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences (IFAS), University of Flroida, Gainesville, FL 32611-0290
  3. Michelle D. Danyluk, assistant professor, Department of Food Science and Human Nutrition, Citrus Research and Education Center, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences (IFAS), University of Florida, Lake Alfred, FL 33850

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